Activated astrocytes enhance the dopaminergic differentiation of stem cells and promote brain repair through bFGF

Nature Communications

Volumn 5, Issue , 2014, Pages

  Yang, Fan ^a   Liu, Yunhui ^a   Tu, Jie ^a   Wan, Jun ^a   Zhang, Jie ^a   Wu, Bifeng ^a   Chen, Shanping ^a   Zhou, Jiawei ^b   Mu, Yangling ^a   Wang, Liping ^a  

^a SHENZHEN INSTITUTES OF ADVANCED TECHNOLOGY   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHANNELRHODOPSIN VARIANT; DOPAMINE; FIBROBLAST GROWTH FACTOR 2; PROTEIN VARIANT; UNCLASSIFIED DRUG; RECOMBINANT PROTEIN; RHODOPSIN;

BRAIN; CELLS AND CELL COMPONENTS; DISEASE TREATMENT; EMBRYONIC DEVELOPMENT; LIGHT EFFECT; NEUROLOGY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; CELL ACTIVATION; CELL REGENERATION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EMBRYO; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO GENE TRANSFER; IN VIVO STUDY; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEURAL STEM CELL TRANSPLANTATION; NONHUMAN; OPTOGENETICS; PARKINSON DISEASE; PHOTOSTIMULATION; PROTEIN SECRETION; SUBSTANTIA NIGRA; UPREGULATION; ANIMAL; BIOLOGICAL THERAPY; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; LIGHT; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PATHOLOGY; PROCEDURES; PROTEIN ENGINEERING; RADIATION RESPONSE; SECRETION (PROCESS); STEM CELL TRANSPLANTATION; TRANSPLANTATION;

ANIMALS; ASTROCYTES; CELL DIFFERENTIATION; CELL- AND TISSUE-BASED THERAPY; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOPAMINERGIC NEURONS; EMBRYONIC STEM CELLS; FIBROBLAST GROWTH FACTOR 2; GENE EXPRESSION REGULATION; HUMANS; LIGHT; MICE; NEURAL STEM CELLS; NEUROGENESIS; PARKINSON DISEASE; PROTEIN ENGINEERING; RECOMBINANT PROTEINS; RHODOPSIN; STEM CELL TRANSPLANTATION; SUBSTANTIA NIGRA;

EID: 84922908850     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6627     Document Type: Article

References (53)

1. Kim, J. H. et al. Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease. Nature 418, 50-56 (2002).
2. Ganat, Y. M. et al. Identification of embryonic stem cell-derived midbrain dopaminergic neurons for engraftment. J. Clin. Invest. 122, 2928-2939 (2012).
3. Kriks, S. et al. Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature 480, 547-551 (2011).
4. Bayly, R. D., Brown, C. Y. &Agarwala, S. A novel role for FOXA2 and SHH in organizing midbrain signaling centers. Dev. Biol. 369, 32-42 (2012).
5. Andersson, E. et al. Identification of intrinsic determinants of midbrain dopamine neurons. Cell 124, 393-405 (2006).
6. L'Episcopo, F. et al. Wnt/beta-catenin signaling is required to rescue midbrain dopaminergic progenitors and promote neurorepair in ageing mouse model of Parkinson's disease. Stem Cells 32, 2147-2163 (2014).
7. Joksimovic, M. &Awatramani, R. Wnt/beta-catenin signaling in midbrain dopaminergic neuron specification and neurogenesis. J. Mol. Cell Biol. 6, 27-33 (2014).
8. Andersson, E. R. et al. Wnt5a cooperates with canonical Wnts to generate midbrain dopaminergic neurons in vivo and in stem cells. Proc. Natl Acad. Sci. USA 110, E602-E610 (2013).
9. Lahti, L., Peltopuro, P., Piepponen, T. P. &Partanen, J. Cell-autonomous FGF signaling regulates anteroposterior patterning and neuronal differentiation in the mesodiencephalic dopaminergic progenitor domain. Development 139, 894-905 (2012).
10. Baron, O., Ratzka, A. &Grothe, C. Fibroblast growth factor 2 regulates adequate nigrostriatal pathway formation in mice. J. Comp. Neurol. 520, 3949-3961 (2012).
11. Ye, W., Shimamura, K., Rubenstein, J. L., Hynes, M. A. &Rosenthal, A. FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell 93, 755-766 (1998).
12. LaVaute, T. M. et al. Regulation of neural specification from human embryonic stem cells by BMP and FGF. Stem Cells 27, 1741-1749 (2009).
13. Cho, M. S., Hwang, D. Y. &Kim, D. W. Efficient derivation of functional dopaminergic neurons from human embryonic stem cells on a large scale. Nat. Protoc. 3, 1888-1894 (2008).
14. Daadi, M. M. &Weiss, S. Generation of tyrosine hydroxylase-producing neurons from precursors of the embryonic and adult forebrain. J. Neurosci. 19, 4484-4497 (1999).
15. Saarimaki-Vire, J. et al. Fibroblast growth factor receptors cooperate to regulate neural progenitor properties in the developing midbrain and hindbrain. J. Neurosci. 27, 8581-8592 (2007).
16. Grothe, C. &Timmer, M. The physiological and pharmacological role of basic fibroblast growth factor in the dopaminergic nigrostriatal system. Brain Res. Rev. 54, 80-91 (2007).
17. Tooyama, I. et al. Loss of basic fibroblast growth factor in substantia nigra neurons in Parkinson's disease. Neurology 43, 372-376 (1993).
18. Timmer, M. et al. Enhanced survival, reinnervation, and functional recovery of intrastriatal dopamine grafts co-transplanted with Schwann cells overexpressing high molecular weight FGF-2 isoforms. Exp. Neurol. 187, 118-136 (2004).
19. Takayama, H. et al. Basic fibroblast growth factor increases dopaminergic graft survival and function in a rat model of Parkinson's disease. Nat. Med. 1, 53-58 (1995).
20. Bean, A. J. et al. Expression of acidic and basic fibroblast growth factors in the substantia nigra of rat, monkey, and human. Proc. Natl Acad. Sci. USA 88, 10237-10241 (1991).
21. Zhang, X. et al. Activation of phosphatidylinositol-linked D1-like receptor modulates FGF-2 expression in astrocytes via IP3-dependent Ca2 signaling. J. Neurosci. 29, 7766-7775 (2009).
22. Robel, S., Berninger, B. &Gotz, M. The stem cell potential of glia: lessons from reactive gliosis. Nat. Rev. Neurosci. 12, 88-104 (2011).
23. Li, K. et al. Ventral mesencephalon astrocytes are more efficient than those of other regions in inducing dopaminergic neurons through higher expression level of TGF-beta3. J. Mol. Neurosci. 37, 288-300 (2009).
24. Song, H., Stevens, C. F. &Gage, F. H. Astroglia induce neurogenesis from adult neural stem cells. Nature 417, 39-44 (2002).
25. Marchetti, B. et al. Uncovering novel actors in astrocyte-neuron crosstalk in Parkinson's disease: the Wnt/beta-catenin signaling cascade as the common final pathway for neuroprotection and self-repair. Eur. J. Neurosci. 37, 1550-1563 (2013).
26. L'Episcopo, F. et al. Reactive astrocytes and Wnt/beta-catenin signaling link nigrostriatal injury to repair in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. Neurobiol. Dis. 41, 508-527 (2011).
27. L'Episcopo, F. et al. A Wnt1 regulated Frizzled-1/beta-Catenin signaling pathway as a candidate regulatory circuit controlling mesencephalic dopaminergic neuron-astrocyte crosstalk: Therapeutical relevance for neuron survival and neuroprotection. Mol. Neurodegener. 6, 49 (2011).
28. Sandhu, J. K. et al. Astrocyte-secreted GDNF and glutathione antioxidant system protect neurons against 6OHDA cytotoxicity. Neurobiol. Dis. 33, 405-414 (2009).
29. Chen, P. C. et al. Nrf2-mediated neuroprotection in the MPTP mouse model of Parkinson's disease: Critical role for the astrocyte. Proc. Natl Acad. Sci. USA 106, 2933-2938 (2009).
30. Chen, P. S. et al. Valproate protects dopaminergic neurons in midbrain neuron/ glia cultures by stimulating the release of neurotrophic factors from astrocytes. Mol. Psychiatry 11, 1116-1125 (2006).
31. Shao, W. et al. Suppression of neuroinflammation by astrocytic dopamine D2 receptors via alphaB-crystallin. Nature 494, 90-94 (2013).
32. Saijo, K. et al. A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death. Cell 137, 47-59 (2009).
33. Roy, N. S. et al. Functional engraftment of human ES cell-derived dopaminergic neurons enriched by coculture with telomerase-immortalized midbrain astrocytes. Nat. Med. 12, 1259-1268 (2006).
34. Ungless, M. A. &Grace, A. A. Are you or aren't you? Challenges associated with physiologically identifying dopamine neurons. Trends. Neurosci. 35, 422-430 (2012).
35. Li, A. et al. Apomorphine-induced activation of dopamine receptors modulates FGF-2 expression in astrocytic cultures and promotes survival of dopaminergic neurons. FASEB J. 20, 1263-1265 (2006).
36. Nomura, T., Goritz, C., Catchpole, T., Henkemeyer, M. &Frisen, J. EphB signaling controls lineage plasticity of adult neural stem cell niche cells. Cell Stem Cell 7, 730-743 (2010).
37. Huang, J., Ye, Z., Hu, X., Lu, L. &Luo, Z. Electrical stimulation induces calcium-dependent release of NGF from cultured Schwann cells. Glia 58, 622-631 (2010).
38. Efetova, M. et al. Separate roles of PKA and EPAC in renal function unraveled by the optogenetic control of cAMP levels in vivo. J. Cell. Sci. 126, 778-788 (2012).
39. Boilly, B., Vercoutter-Edouart, A. S., Hondermarck, H., Nurcombe, V. &Le Bourhis, X. FGF signals for cell proliferation and migration through different pathways. Cytokine Growth Factor Rev. 11, 295-302 (2000).
40. Villegas, S. N., Canham, M. &Brickman, J. M. FGF signalling as a mediator of lineage transitions-evidence from embryonic stem cell differentiation. J. Cell. Biochem. 110, 10-20 (2010).
41. Stavridis, M. P., Lunn, J. S., Collins, B. J. &Storey, K. G. A discrete period of FGF-induced Erk1/2 signalling is required for vertebrate neural specification. Development 134, 2889-2894 (2007).
42. Chakkalakal, J. V., Jones, K. M., Basson, M. A. &Brack, A. S. The aged niche disrupts muscle stem cell quiescence. Nature 490, 355-360 (2012).
43. Peng, J., Xie, L., Jin, K., Greenberg, D. A. &Andersen, J. K. Fibroblast growth factor 2 enhances striatal and nigral neurogenesis in the acute 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. Neuroscience 153, 664-670 (2008).
44. Timmer, M. et al. Fibroblast growth factor (FGF)-2 and FGF receptor 3 are required for the development of the substantia nigra, and FGF-2 plays a crucial role for the rescue of dopaminergic neurons after 6-hydroxydopamine lesion. J. Neurosci. 27, 459-471 (2007).
45. Jensen, P., Pedersen, E. G., Zimmer, J., Widmer, H. R. &Meyer, M. Functional effect of FGF2-and FGF8-expanded ventral mesencephalic precursor cells in a rat model of Parkinson's disease. Brain Res. 1218, 13-20 (2008).
46. Tu, J. et al. Light-controlled astrocytes promote human mesenchymal stem cells toward neuronal differentiation and improve the neurological deficit in stroke rats. Glia 62, 106-121 (2014).
47. Chen, J. et al. Heterosynaptic long-term depression mediated by ATP released from astrocytes. Glia 61, 178-191 (2013).
48. Sasaki, T. et al. Application of an optogenetic byway for perturbing neuronal activity via glial photostimulation. Proc. Natl Acad. Sci. USA 109, 20720-20725 (2012).
49. Gourine, A. V. et al. Astrocytes control breathing through pH-dependent release of ATP. Science 329, 571-575 (2010).
50. Perea, G., Yang, A., Boyden, E. S. &Sur, M. Optogenetic astrocyte activation modulates response selectivity of visual cortex neurons in vivo. Nat. Commun. 5, 3262 (2014).
51. Beppu, K. et al. Optogenetic countering of glial acidosis suppresses glial glutamate release and ischemic brain damage. Neuron 81, 314-320 (2014).
52. Chen, X. et al. Disrupted and transgenic urate oxidase alter urate and dopaminergic neurodegeneration. Proc. Natl Acad. Sci. USA 110, 300-305 (2013).
53. Xiao, D. et al. Forebrain adenosine A2A receptors contribute to L-3,4-dihydroxyphenylalanine-induced dyskinesia in hemiparkinsonian mice. J. Neurosci. 26, 13548-13555 (2006).