Persistent astrocyte activation in the fragile X mouse cerebellum

Brain and Behavior

Volumn 5, Issue 10, 2015, Pages

  Pacey, Laura K K ^a   Guan, Sihui ^a   Tharmalingam, Sujeenthar ^a   Thomsen, Christian ^b   Hampson, David R ^a,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b LUNDBECK RESEARCH USA   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Astrogliosis; Autism; FMRP; GFAP; LIF; Myelin; Oligodendrocyte precursor cells; S100B; TNFR2

Indexed keywords

FRAGILE X MENTAL RETARDATION PROTEIN; LEUKEMIA INHIBITORY FACTOR; TUMOR NECROSIS FACTOR RECEPTOR 2; FMR1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; ASTROCYTE ACTIVATION; BRAIN SIZE; CEREBELLUM; CONTROLLED STUDY; EVOKED RESPONSE; FRAGILE X SYNDROME; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; WESTERN BLOTTING; ANIMAL; AUTISM; DISEASE MODEL; FEMALE; GENETICS; GLIA; KNOCKOUT MOUSE; METABOLISM; MICROGLIA; NERVE CELL; PATHOLOGY;

ANIMALS; ASTROCYTES; AUTISTIC DISORDER; CEREBELLUM; DISEASE MODELS, ANIMAL; FEMALE; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; MICE; MICE, KNOCKOUT; MICROGLIA; NEUROGLIA; NEURONS;

EID: 84945242993     PISSN: None     EISSN: 21623279     Source Type: Journal    
DOI: 10.1002/brb3.400     Document Type: Article

References (50)

1. Adusei, D. C., L. K. Pacey, D. Chen, and D. R. Hampson . 2010. Early developmental alterations in GABAergic protein expression in fragile X knockout mice. Neuropharmacology 59:167-171.
2. Ascano, M., Jr., N. Mukherjee, P. Bandaru, J. B. Miller, J. D. Nusbaum, D. L. Corcoran, et al. 2012. FMRP targets distinct mRNA sequence elements to regulate protein expression. Nature 492:382-386.
3. Ashwood, P., D. V. Nguyen, D. Hessl, R. J. Hagerman, and F. Tassone . 2010. Plasma cytokine profiles in Fragile X subjects: is there a role for cytokines in the pathogenesis? Brain Behav. Immun. 24:898-902.
4. Ashwood, P., P. Krakowiak, I. Hertz-Picciotto, R. Hansen, I. Pessah, and J. Van de Water . 2011. Elevated plasma cytokines in autism spectrum disorders provide evidence of immune dysfunction and are associated with impaired behavioral outcome. Brain Behav. Immun. 25:40-45.
5. Bagni, C., and B. A. Oostra . 2013. Fragile X syndrome: from protein function to therapy. Am. J. Med. Genet. A 161A:2809-2821.
6. Bal-Price, A., and G. C. Brown . 2001. Inflammatory neurodegeneration mediated by nitric oxide from activated glia-inhibiting neuronal respiration, causing glutamate release and excitotoxicity. J. Neurosci. 21:6480-6491.
7. Bilousova, T. V., L. Dansie, M. Ngo, J. Aye, J. R. Charles, D. W. Ethell, et al. 2009. Minocycline promotes dendritic spine maturation and improves behavioural performance in the fragile X mouse model. J. Med. Genet. 46:94-102.
8. Callan, M. A., N. Clements, N. Ahrendt, and D. C. Zarnescu . 2012. Fragile X protein is required for inhibition of insulin signaling and regulates glial-dependent neuroblast reactivation in the developing brain. Brain Res. 1462:151-161.
9. Cao, Z., S. Hulsizer, Y. Cui, D. L. Pretto, K. H. Kim, P. J. Hagerman, et al. 2013. Enhanced asynchronous Ca(2+) oscillations associated with impaired glutamate transport in cortical astrocytes expressing Fmr1 gene premutation expansion. J. Biol. Chem. 288:13831-13841.
10. Carbone, D. L., J. A. Moreno, and R. B. Tjalkens . 2008. Nuclear factor kappa-B mediates selective induction of neuronal nitric oxide synthase in astrocytes during low-level inflammatory stimulation with MPTP. Brain Res. 1217:1-9.
11. Careaga, M., T. Noyon, K. Basuta, J. Van de Water, F. Tassone, R. J. Hagerman, et al. 2014. Group I metabotropic glutamate receptor mediated dynamic immune dysfunction in children with fragile X syndrome. J. Neuroinflammation 11:110.
12. Catania, M. V., R. Giuffrida, G. Seminara, G. Barbagallo, E. Aronica, J. A. Gorter, et al. 2003. Upregulation of neuronal nitric oxide synthase in in vitro stellate astrocytes and in vivo reactive astrocytes after electrically induced status epilepticus. Neurochem. Res. 28:607-615.
13. Darnell, J. C., S. J. Van Driesche, C. Zhang, K. Y. Hung, A. Mele, C. E. Fraser, et al. 2011. FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 146:247-261.
14. Edmonson, C., M. N. Ziats, and O. M. Rennert . 2014. Altered glial marker expression in autistic post-mortem prefrontal cortex and cerebellum. Mol. Autism 5:3.
15. Fischer, R., O. Maier, M. Siegemund, H. Wajant, P. Scheurich, and K. Pfizenmaier . 2011. A TNF receptor 2 selective agonist rescues human neurons from oxidative stress-induced cell death. PLoS One 6:e27621.
16. Fischer, R., H. Wajant, R. Kontermann, K. Pfizenmaier, and O. Maier . 2014. Astrocyte-specific activation of TNFR2 promotes oligodendrocyte maturation by secretion of leukemia inhibitory factor. Glia 62:272-283.
17. Forbes-Lorman, R. M., J. R. Kurian, and A. P. Auger . 2014. MeCP2 regulates GFAP expression within the developing brain. Brain Res. 1543:151-158.
18. Gholizadeh, S., S. K. Halder, and D. R. Hampson . 2015. Expression of fragile X mental retardation protein in neurons and glia of the developing and adult mouse brain. Brain Res. 1596:22-30.
19. Giampetruzzi, A., J. H. Carson, and E. Barbarese . 2013. FMRP and myelin protein expression in oligodendrocytes. Mol. Cell Neurosci. 56:333-341.
20. Gkogkas, C. G., A. Khoutorsky, R. Cao, S. M. Jafarnejad, M. Prager-Khoutorsky, N. Giannakas, et al. 2014. Pharmacogenetic inhibition of eIF4E-dependent Mmp9 mRNA translation reverses fragile X syndrome-like phenotypes. Cell Rep. 9:1742-1755.
21. Goines, P., and J. Van de Water . 2010. The immune system's role in the biology of autism. Curr. Opin. Neurol. 23:111-117.
22. Gross, C., M. Nakamoto, X. Yao, C. B. Chan, S. Y. Yim, K. Ye, et al. 2010. Excess phosphoinositide 3-kinase subunit synthesis and activity as a novel therapeutic target in fragile X syndrome. J. Neurosci. 30:10624-10638.
23. Hagerman, R., G. Hoem, and P. Hagerman . 2010. Fragile X and autism: intertwined at the molecular level leading to targeted treatments. Mol. Autism 1:12.
24. Hampson, D. R., S. Gholizadeh, and L. K. Pacey . 2012. Pathways to drug development for autism spectrum disorders. Clin. Pharmacol. Ther. 91:189-200.
25. Higashimori, H., L. Morel, J. Huth, L. Lindemann, C. Dulla, A. Taylor, et al. 2013. Astroglial FMRP-dependent translational down-regulation of mGluR5 underlies glutamate transporter GLT1 dysregulation in the fragile X mouse. Hum. Mol. Genet. 22:2041-2054.
26. Ishibashi, T., K. A. Dakin, B. Stevens, P. R. Lee, S. V. Kozlov, C. L. Stewart, et al. 2006. Astrocytes promote myelination in response to electrical impulses. Neuron 49:823-832.
27. Jacobs, S., and L. C. Doering . 2010. Astrocytes prevent abnormal neuronal development in the fragile x mouse. J. Neurosci. 30:4508-4514.
28. Jacobs, S., M. Nathwani, and L. C. Doering . 2010. Fragile X astrocytes induce developmental delays in dendrite maturation and synaptic protein expression. BMC Neurosci. 11:132.
29. Lee, Y. B., S. Du, H. Rhim, E. B. Lee, G. J. Markelonis, and T. H. Oh . 2000. Rapid increase in immunoreactivity to GFAP in astrocytes in vitro induced by acidic pH is mediated by calcium influx and calpain I. Brain Res. 864:220-229.
30. Li, X., A. Chauhan, A. M. Sheikh, S. Patil, V. Chauhan, X. M. Li, et al. 2009. Elevated immune response in the brain of autistic patients. J. Neuroimmunol. 207:111-116.
31. Liedtke, W., W. Edelmann, P. L. Bieri, F. C. Chiu, N. J. Cowan, R. Kucherlapati, et al. 1996. GFAP is necessary for the integrity of CNS white matter architecture and long-term maintenance of myelination. Neuron 17:607-615.
32. Luth, H. J., M. Holzer, U. Gartner, M. Staufenbiel, and T. Arendt . 2001. Expression of endothelial and inducible NOS-isoforms is increased in Alzheimer's disease, in APP23 transgenic mice and after experimental brain lesion in rat: evidence for an induction by amyloid pathology. Brain Res. 913:57-67.
33. Molofsky, A. V., R. Krencik, E. M. Ullian, H. H. Tsai, B. Deneen, W. D. Richardson, et al. 2012. Astrocytes and disease: a neurodevelopmental perspective. Genes Dev. 26:891-907.
34. Naude, P. J., J. A. den Boer, P. G. Luiten, and U. L. Eisel . 2011. Tumor necrosis factor receptor cross-talk. FEBS J. 278:888-898.
35. Noble, L. J., F. Donovan, T. Igarashi, S. Goussev, and Z. Werb . 2002. Matrix metalloproteinases limit functional recovery after spinal cord injury by modulation of early vascular events. J. Neurosci. 22:7526-7535.
36. Onore, C., J. Van de Water, and P. Ashwood . 2012. Decreased levels of EGF in plasma of children with autism spectrum disorder. Autism Res. Treat. 2012:205362.
37. Pacey, L. K., and L. C. Doering . 2007. Developmental expression of FMRP in the astrocyte lineage: implications for fragile X syndrome. Glia 55:1601-1609.
38. Pacey, L. K., I. C. Xuan, S. Guan, D. Sussman, R. M. Henkelman, Y. Chen, et al. 2013. Delayed myelination in a mouse model of fragile X syndrome. Hum. Mol. Genet. 22:3920-3930.
39. Pekny, M., and M. Pekna . 2014. Astrocyte reactivity and reactive astrogliosis: costs and benefits. Physiol. Rev. 94:1077-1098.
40. Pekny, M., U. Wilhelmsson, and M. Pekna . 2014. The dual role of astrocyte activation and reactive gliosis. Neurosci. Lett. 565:30-38.
41. Sethna, F., C. Moon, and H. Wang . 2014. From FMRP function to potential therapies for fragile X syndrome. Neurochem. Res. 39:1016-1031.
42. Sidhu, H., L. E. Dansie, P. W. Hickmott, D. W. Ethell, and I. M. Ethell . 2014. Genetic removal of matrix metalloproteinase 9 rescues the symptoms of fragile X syndrome in a mouse model. J. Neurosci. 34:9867-9879.
43. Siman, R., J. P. Card, R. B. Nelson, and L. G. Davis . 1989. Expression of beta-amyloid precursor protein in reactive astrocytes following neuronal damage. Neuron 3:275-285.
44. Tessier, C. R., and K. Broadie . 2011. The fragile X mental retardation protein developmentally regulates the strength and fidelity of calcium signaling in Drosophila mushroom body neurons. Neurobiol. Dis. 41:147-159.
45. Vargas, D. L., C. Nascimbene, C. Krishnan, A. W. Zimmerman, and C. A. Pardo . 2005. Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann. Neurol. 57:67-81.
46. Wang, J., and R. S. Al-Lamki . 2013. Tumor necrosis factor receptor 2: its contribution to acute cellular rejection and clear cell renal carcinoma. Biomed Res. Int. 2013:821310.
47. Wang, H., L. Ku, D. J. Osterhout, W. Li, A. Ahmadian, Z. Liang, et al. 2004. Developmentally-programmed FMRP expression in oligodendrocytes: a potential role of FMRP in regulating translation in oligodendroglia progenitors. Hum. Mol. Genet. 13:79-89.
48. Westmark, C. J., P. R. Westmark, K. J. O'Riordan, B. C. Ray, C. M. Hervey, M. S. Salamat, et al. 2011. Reversal of fragile X phenotypes by manipulation of AbetaPP/Abeta levels in Fmr1KO mice. PLoS One 6:e26549.
49. Yang, Q., B. Feng, K. Zhang, Y. Y. Guo, S. B. Liu, Y. M. Wu, et al. 2012. Excessive astrocyte-derived neurotrophin-3 contributes to the abnormal neuronal dendritic development in a mouse model of fragile X syndrome. PLoS Genet. 8:e1003172.
50. Yuskaitis, C. J., E. Beurel, and R. S. Jope . 2010. Evidence of reactive astrocytes but not peripheral immune system activation in a mouse model of Fragile X syndrome. Biochim. Biophys. Acta 1802:1006-1012.