Astrocyte development: A Guide for the Perplexed

GLIA

Volumn 63, Issue 8, 2015, Pages 1320-1329

  Molofsky, Anna Victoria ^a   Deneen, Benjamin ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Glia; Gliogenesis; Neurogenesis; Neuroglia; Patterning

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 3; NEUROTRANSMITTER; STAT3 PROTEIN;

ASTROCYTE; ASTROCYTE CULTURE; ASTROCYTOSIS; BIODIVERSITY; BRAIN CANCER; BRAIN FUNCTION; BRAIN REGION; CELL FATE; CELL HETEROGENEITY; CELL MANIPULATION; CELL MATURATION; CELL MIGRATION; CELL STRUCTURE; CENTRAL NERVOUS SYSTEM; DEGENERATIVE DISEASE; ENVIRONMENTAL FACTOR; GLUTAMATERGIC SYNAPSE; HUMAN; MACROGLIA; METABOLIC REGULATION; MOLECULAR BIOLOGY; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROIMMUNOLOGY; NEUROLOGIC DISEASE; NEUROPHYSIOLOGY; NEUROTRANSMISSION; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN EXPRESSION; RABBIT; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; ANIMAL; CELL PROLIFERATION; CYTOLOGY; PHYSIOLOGY;

ANIMALS; ASTROCYTES; CELL PROLIFERATION; HUMANS; NEURAL STEM CELLS;

EID: 84930869090     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22836     Document Type: Review

References (87)

1. Allaman I, Bélanger M, Magistretti PJ. 2011. Astrocyte-neuron metabolic relationships: For better and for worse. Trends Neurosci 34:76-87.
2. Allen NJ, Barres BA. 2009. Neuroscience: Glia-more than just brain glue. Nature 457:675-677.
3. Anthony TE, Klein C, Fishell G, Heintz N. 2004. Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 41:881-890.
4. Ballas N, Lioy DT, Grunseich C, Mandel G. 2009. Non-cell autonomous influence of MeCP2-deficient glia on neuronal dendritic morphology. Nat Neurosci 12:311-317.
5. Bandeira F, Lent R, Herculano-Houzel S. 2009. Changing numbers of neuronal and non-neuronal cells underlie postnatal brain growth in the rat. Proc Natl Acad Sci U S A 106:14108-14113.
6. Barnabé-Heider F, Wasylnka JA, Fernandes KJL, Porsche C, Sendtner M, Kaplan DR, Miller FD. 2005. Evidence that embryonic neurons regulate the onset of cortical gliogenesis via cardiotrophin-1. Neuron 48:253-265.
7. Berninger B, Costa MR, Koch U, Schroeder T, Sutor B, Grothe B, Götz M. 2007. Functional properties of neurons derived from in vitro reprogrammed postnatal astroglia. J Neurosci 27:8654-8664.
8. Bradford J, Shin J-Y, Roberts M, Wang C-E, Li X-J, Li S. 2009. Expression of mutant huntingtin in mouse brain astrocytes causes age-dependent neurological symptoms. Proc Natl Acad Sci U S A 106:22480-22485.
9. Bushong EA, Martone ME, Ellisman MH. 2003. Examination of the relationship between astrocyte morphology and laminar boundaries in the molecular layer of adult dentate gyrus. J Comp Neurol 462:241-251.
10. Bushong EA, Martone ME, Ellisman MH. 2004. Maturation of astrocyte morphology and the establishment of astrocyte domains during postnatal hippocampal development. Int J Dev Neurosci 22:73-86.
11. Clarke LE, Barres BA. 2013. Emerging roles of astrocytes in neural circuit development. Nat Rev Neurosci 14:311-321.
12. Deneen B, Ho R, Lukaszewicz A, Hochstim CJ, Gronostajski RM, Anderson DJ. 2006. The transcription factor NFIA controls the onset of gliogenesis in the developing spinal cord. Neuron 52:953-968.
13. Doetsch F, Caillé I, Lim DA, García-Verdugo JM, Alvarez-Buylla A. 1999. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703-716.
14. Elmariah SB, Oh EJ, Hughes EG, Balice-Gordon RJ. 2005. Astrocytes regulate inhibitory synapse formation via Trk-mediated modulation of postsynaptic GABAA receptors. J Neurosci 25:3638-3650.
15. Etienne-Manneville S. 2006. In vitro assay of primary astrocyte migration as a tool to study rho GTPase function in cell polarization. Meth Enzymol 406:565-578.
16. Fleming JT, He W, Hao C, Ketova T, Pan FC, Wright CCV, Litingtung Y, Chiang C. 2013. The purkinje neuron acts as a central regulator of spatially and functionally distinct cerebellar precursors. Dev Cell 27:278-292.
17. Foo LC, Allen NJ, Bushong EA, Ventura PB, Chung W-S, Zhou L, Cahoy JD, Daneman R, Zong H, Ellisman MH, Barres BA. 2011. Development of a method for the purification and culture of rodent astrocytes. Neuron 71:799-811.
18. Foo LC, Dougherty JD. 2013. Aldh1L1 is expressed by postnatal neural stem cells in vivo. Glia 61:1533-1541.
19. Franzdóttir SR, Engelen D, Yuva-Aydemir Y, Schmidt I, Aho A, Klämbt C. 2009. Switch in FGF signalling initiates glial differentiation in the drosophila eye. Nature 460:758-761.
20. Freeman MR, Rowitch DH. 2013. Evolving concepts of gliogenesis: A look way back and ahead to the next 25 years. Neuron 80:613-623.
21. Freeman MR. 2010. Specification and morphogenesis of astrocytes. Science 330:774-778.
22. Ge W-P, Miyawaki A, Gage FH, Jan Y-N, Jan LY. 2012. Local generation of glia is a major astrocyte source in postnatal cortex. Nature 484:376-380.
23. Gomes FC, Paulin D, Moura Neto V. 1999. Glial fibrillary acidic protein (GFAP): modulation by growth factors and its implication in astrocyte differentiation. Braz J Med Biol Res 32:619-631.
24. Gomes WA, Mehler MF, Kessler JA. 2003. Transgenic overexpression of bmp4 increases astroglial and decreases oligodendroglial lineage commitment. Dev Biol 255:164-177.
25. Gourine AV, Kasymov V, Marina N, Tang F, Figueiredo MF, Lane S, Teschemacher AG, Spyer KM, Deisseroth K, Kasparov S. 2010. Astrocytes control breathing through pH-dependent release of ATP. Science 329:571-575.
26. Hamilton NB, Attwell D. 2010. Do astrocytes really exocytose neurotransmitters? Nat Rev Neurosci 11:227-238.
27. Heins N, Malatesta P, Cecconi F, Nakafuku M, Tucker KL, Hack MA, Chapouton P, Barde Y-A, Götz M. 2002. Glial cells generate neurons: The role of the transcription factor pax6. Nat Neurosci 5:308-315.
28. Hochstim C, Deneen B, Lukaszewicz A, Zhou Q, Anderson DJ. 2008. Identification of positionally distinct astrocyte subtypes whose identities are specified by a homeodomain code. Cell 133:510-522.
29. Hosoya T, Takizawa K, Nitta K, Hotta Y. 1995. Glial cells missing: A binary switch between neuronal and glial determination in drosophila. Cell 82:1025-1036.
30. Jacobsen CT, Miller RH. 2003. Control of astrocyte migration in the developing cerebral cortex. Dev Neurosci 25:207-216.
31. Jessell TM. 2000. Neuronal specification in the spinal cord: Inductive signals and transcriptional codes. Nat Rev Genet 1:20-29.
32. JohnLin C-C, Deneen B. 2013. Astrocytes: The missing link in neurologic disease? Semin Pediatr Neurol 20:236-241.
33. Jones BW, Fetter RD, Tear G, Goodman CS. 1995. Glial cells missing: A genetic switch that controls glial versus neuronal fate. Cell 82:1013-1023.
34. Kang P, Lee HK, Glasgow SM, Finley M, Donti T, Gaber ZB, Graham BH, Foster AE, Novitch BG, Gronostajski RM, Deneen B. 2011. sox9 and NFIA coordinate a transcriptional regulatory cascade during the initiation of gliogenesis. Neuron [Internet] 74:79-94. Available at: http://linkinghub.elsevier.com/retrieve/pii/S0896627312001420
35. Kim J, Jones BW, Zock C, Chen Z, Wang H, Goodman CS, Anderson DJ. 1998. Isolation and characterization of mammalian homologs of the drosophila gene glial cells missing. Proc Natl Acad Sci U S A 95:12364-12369.
36. Kriegstein A, Alvarez-Buylla A. 2009. The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32:149-184.
37. Li X, Newbern JM, Wu Y, Morgan-Smith M, Zhong J, Charron J, Snider WD. 2012. MEK is a key regulator of gliogenesis in the developing brain. Neuron 75:1035-1050.
38. Lioy DT, Garg SK, Monaghan CE, Raber J, Foust KD, Kaspar BK, Hirrlinger PG, Kirchhoff F, Bissonnette JM, Ballas N, Mandel G. 2011. A role for glia in the progression of rett's syndrome. Nature 475:497-500.
39. Lister R, Mukamel EA, Nery JR, Urich M, Puddifoot CA, Johnson ND, Lucero J, Huang Y, Dwork AJ, Schultz MD, Yu M, Tonti-Filippini J, Heyn H, Hu S, Wu JC, Rao A, Esteller M, He C, Haghighi FG, Sejnowski TJ, Behrens MM, Ecker JR. 2013. Global epigenomic reconfiguration during mammalian brain development. Science 341:1237905.
40. Louvi A, Artavanis-Tsakonas S. 2006. Notch signalling in vertebrate neural development. Nat Rev Neurosci 7:93-102.
41. López-Hidalgo M, Schummers J. 2014. Cortical maps: A role for astrocytes? Curr Opin Neurobiol 24:176-189.
42. Magavi S, Friedmann D, Banks G, Stolfi A, Lois C. 2012. Coincident generation of pyramidal neurons and protoplasmic astrocytes in neocortical columns. J Neurosci 32:4762-4772.
43. Magnusson JP, Göritz C, Tatarishvili J, Dias DO, Smith EMK, Lindvall O, Kokaia Z, Frisén J. 2014. A latent neurogenic program in astrocytes regulated by notch signaling in the mouse. Science 346:237-241.
44. Marazziti D, Di Pietro C, Golini E, Mandillo S, La Sala G, Matteoni R, Tocchini-Valentini GP. 2013. Precocious cerebellum development and improved motor functions in mice lacking the astrocyte cilium-, patched 1-associated gpr37l1 receptor. Proc Natl Acad Sci U S A 110:16486-16491.
45. Masahira N, Takebayashi H, Ono K, Watanabe K, Ding L, Furusho M, Ogawa Y, Nabeshima Y-I, Alvarez-Buylla A, Shimizu K, Ikenaka K. 2006. Olig2-positive progenitors in the embryonic spinal cord give rise not only to motoneurons and oligodendrocytes, but also to a subset of astrocytes and ependymal cells. Dev Biol 293:358-369.
46. Matyash V, Kettenmann H. 2010. Heterogeneity in astrocyte morphology and physiology. Brain Res Rev 63:2-10.
47. Mich JK, Signer RA, Nakada D, Pineda A, Burgess RJ, Vue TY, Johnson JE, Morrison SJ. 2014. Prospective identification of functionally distinct stem cells and neurosphere-initiating cells in adult mouse forebrain. Elife 3:e02669.
48. Middeldorp J, Hol EM. 2011. GFAP in health and disease. Prog Neurobiol 93:421-443.
49. Miller RH. 2002. Regulation of oligodendrocyte development in the vertebrate CNS. Prog Neurobiol 67:451-467.
50. Molofsky AV, Glasgow SM, Chaboub LS, Tsai HH, Murnen AT, Kelley KW, Fancy SPJ, Yuen TJ, Madireddy L, Baranzini S, Deneen B, Rowitch DH, Oldham MC. 2013a. Expression profiling of Aldh1l1-precursors in the developing spinal cord reveals glial lineage-specific genes and direct Sox9-nfe2l1 interactions. Glia 61:1518-1532.
51. Molofsky AV, Hochstim C, Deneen B, Rowitch D. 2013b. Mechanisms of Astrocyte development. Elsevier. pp 723-742.
52. Molofsky AV, Kelley KW, Tsai HH, Redmond SA, Chang SM, Madireddy L, Chan JR, Baranzini SE, Ullian EM, Rowitch DH. 2014. Astrocyte-encoded positional cues maintain sensorimotor circuit integrity. Nature 509:189-194.
53. Molofsky AV, Krenick R, Ullian E, Tsai HH, Deneen B, Richardson WD, Barres BA, Rowitch DH. 2012. Astrocytes and disease: A neurodevelopmental perspective. Genes Dev 26:891-907.
54. Muroyama Y, Fujiwara Y, Orkin SH, Rowitch DH. 2005. Specification of astrocytes by bHLH protein SCL in a restricted region of the neural tube. Nature 438:360-363.
55. Muthukumar AK, Stork T, Freeman MR. 2014. Activity-dependent regulation of astrocyte GAT levels during synaptogenesis. Nat Neurosci 17:1340-1350.
56. Namihira M, Kohyama J, Semi K, Sanosaka T, Deneen B, Taga T, Nakashima K. 2009. Committed neuronal precursors confer astrocytic potential on residual neural precursor cells. Dev Cell 16:245-255.
57. Niu W, Zang T, Zou Y, Fang S, Smith DK, Bachoo R, Zhang C-L. 2013. In vivo reprogramming of astrocytes to neuroblasts in the adult brain. Nat Cell Biol 15:1164-1175.
58. Oh LYS, Denninger A, Colvin JS, Vyas A, Tole S, Ornitz DM, Bansal R. 2003. Fibroblast growth factor receptor 3 signaling regulates the onset of oligodendrocyte terminal differentiation. J Neurosci 23:883-894.
59. Osmani N, Vitale N, Borg J-P, Etienne-Manneville S. 2006. Scrib controls cdc42 localization and activity to promote cell polarization during astrocyte migration. Curr Biol 16:2395-2405.
60. Owada Y, Yoshimoto T, Kondo H. 1996. Spatio-temporally differential expression of genes for three members of fatty acid binding proteins in developing and mature rat brains. J Chem Neuroanat 12:113-122.
61. Placone AL, McGuiggan PM, Bergles DE, Guerrero-Cazares H, Quiñones-Hinojosa A, Searson PC. 2015. Human astrocytes develop physiological morphology and remain quiescent in a novel 3D matrix. Biomaterials 42:134-143.
62. Pringle NP, Yu W-P, Howell M, Colvin JS, Ornitz DM, Richardson WD. 2003. Fgfr3 expression by astrocytes and their precursors: Evidence that astrocytes and oligodendrocytes originate in distinct neuroepithelial domains. Development 130:93-102.
63. Puschmann TB, Zandén C, De Pablo Y, Kirchhoff F, Pekna M, Liu J, Pekny M. 2013. Bioactive 3D cell culture system minimizes cellular stress and maintains the in vivo-like morphological complexity of astroglial cells. Glia 61:432-440.
64. Reichenbach A, Derouiche A, Kirchhoff F. 2010. Morphology and dynamics of perisynaptic glia. Brain Res Rev 63:11-25.
65. Rowitch DH, Kriegstein AR. 2010. Developmental genetics of vertebrate glial-cell specification. Nature 468:214-222.
66. Scholze AR, Foo LC, Mulinyawe S, Barres BA. 2014. BMP signaling in astrocytes downregulates EGFR to modulate survival and maturation. PLoS ONE 9:e110668-
67. Scott CE, Wynn SL, Sesay A, Cruz C, Cheung M, Gomez Gaviro M-V, Booth S, Gao B, Cheah KSE, Lovell-Badge R, Briscoe J. 2010. Sox9 induces and maintains neural stem cells. Nat Neurosci 13:1181-1189.
68. Shenoy A, Danial M, Blelloch RH. 2015. Let-7 and miR-125 cooperate to prime progenitors for astrogliogenesis. EMBO J pii:e201489504.
69. Shibata T, Yamada K, Watanabe M, Ikenaka K, Wada K, Tanaka K, Inoue Y. 1997. Glutamate transporter GLAST is expressed in the radial glia-astrocyte lineage of developing mouse spinal cord. J Neurosci 17:9212-9219.
70. Shin J-Y, Fang Z-H, Yu Z-X, Wang C-E, Li S-H, Li X-J. 2005. Expression of mutant huntingtin in glial cells contributes to neuronal excitotoxicity. J Cell Biol 171:1001-1012.
71. Stolt CC, Lommes P, Sock E, Chaboissier M-C, Schedl A, Wegner M. 2003. The sox9 transcription factor determines glial fate choice in the developing spinal cord. Genes Dev 17:1677-1689.
72. Stork T, Sheehan A, Tasdemir-Yilmaz OE, Freeman MR. 2014. Neuron-glia interactions through the heartless FGF receptor signaling pathway mediate morphogenesis of drosophila astrocytes. Neuron 83:388-403.
73. Su Z, Niu W, Liu M-L, Zou Y, Zhang C-L. 2014. In vivo conversion of astrocytes to neurons in the injured adult spinal cord. Nat Commun 5:3338.
74. Tidyman WE, Rauen KA. 2009. The RASopathies: Developmental syndromes of ras/MAPK pathway dysregulation. Curr Opin Genet Dev 19:230-236.
75. Tien A-C, Tsai HH, Molofsky AV, McMahon M, Foo LC, Kaul A, Dougherty JD, Heintz N, Gutmann DH, Barres BA, Rowitch DH. 2012. Regulated temporal-spatial astrocyte precursor cell proliferation involves BRAF signalling in mammalian spinal cord. Development 139:2477-2487.
76. Tong X, Ao Y, Faas GC, Nwaobi SE, Xu J, Haustein MD, Anderson MA, Mody I, Olsen ML, Sofroniew MV, Khakh BS. 2014. Astrocyte kir4.1 ion channel deficits contribute to neuronal dysfunction in huntington's disease model mice. Nat Neurosci 17:694-703.
77. Tong X, Shigetomi E, Looger LL, Khakh BS. 2013. Genetically encoded calcium indicators and astrocyte calcium microdomains. The Neuroscientist 19:274-291.
78. Torper O, Pfisterer U, Wolf DA, Pereira M, Lau S, Jakobsson J, Björklund A, Grealish S, Parmar M. 2013. Generation of induced neurons via direct conversion in vivo. Proc Natl Acad Sci U S A 110:7038-7043.
79. Tsai HH, Li H, Fuentealba LC, Molofsky AV, Taveira-Marques R, Zhuang H, Tenney A, Murnen AT, Fancy SPJ, Merkle F, Kessaris N, Alvarez-Buylla A, Richardson WD, Rowitch DH. 2012. Regional astrocyte allocation regulates CNS synaptogenesis and repair. Science 337:358-362.
80. Ulloa F, Briscoe J. 2007. Morphogens and the control of cell proliferation and patterning in the spinal cord. Cell Cycle 6:2640-2649.
81. Vue TY, Kim EJ, Parras CM, Guillemot F, Johnson JE. 2014. Ascl1 controls the number and distribution of astrocytes and oligodendrocytes in the gray matter and white matter of the spinal cord. Development 141:3721-3731.
82. Walker FO. 2007. Huntington's disease. Lancet 369:218-228.
83. Yu Y-C, Bultje RS, Wang X, Shi S-H. 2009. Specific synapses develop preferentially among sister excitatory neurons in the neocortex. Nature 458:501-504.
84. Yu Y-C, He S, Chen S, Fu Y, Brown KN, Yao X-H, Ma J, Gao KP, Sosinsky GE, Huang K, Shi S-H. 2012. Preferential electrical coupling regulates neocortical lineage-dependent microcircuit assembly. Nature 486:113-117.
85. Zhao X, Chen Y, Zhu Q, Huang H, Teng P, Zheng K, Hu X, Xie B, Zhang Z, Sander M, Qiu M. 2014. Control of astrocyte progenitor specification, migration and maturation by nkx6.1 homeodomain transcription factor. PLoS ONE 9:e109171.
86. Zhuo L, Theis M, Alvarez-Maya I, Brenner M, Willecke K, Messing A. 2001. hGFAP-cre transgenic mice for manipulation of glial and neuronal function in vivo. Genesis 31:85-94.
87. Zoghbi HY. 2009. Rett syndrome: What do we know for sure? Nat Neurosci 12:239-240.