Animal cells and systems

The Korean Society for Integrative Biology (한국통합생물학회)
권호 표지
DOI QR코드

DOI QR Code

Different expression of human GFAP promoter-derived GFP in different subsets of astrocytes in the mouse brain

  • Moon, Young-Hye (Department of Anatomy, BK21 program, Korea University College of Medicine) ;
  • Kim, Hyun-Jung (Department of Anatomy, BK21 program, Korea University College of Medicine) ;
  • Kim, Joo-Yeon (Department of Anatomy, BK21 program, Korea University College of Medicine) ;
  • Kim, Hyun (Department of Anatomy, BK21 program, Korea University College of Medicine) ;
  • Kim, Woon-Ryoung (Department of Anatomy, BK21 program, Korea University College of Medicine) ;
  • Sun, Woong (Department of Anatomy, BK21 program, Korea University College of Medicine)
  • Received : 2011.04.08
  • Accepted : 2011.07.10
  • Published : 2011.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Transgenic mice expressing green fluorescent protein (GFP) under the control of human glial fibrillary acidic protein promoter (hGFAP) have been utilized for in vivo labeling of astrocytes. Although it has been considered that virtually all astrocytes express GFP in this transgenic mouse, we found that different subsets of GFAP-expressing astrocytes express considerably different levels of GFP in the adult brain. Astrocytes in the spinal cord, the molecular layer of thecerebellum, meninges, white matter, corpus callosum and blood vessels exhibited strong GFP, whereas subsets of astrocytes associated with granule cells in the cerebellum and dentate gyrus did not or only marginally exhibited GFP. We also found that a small subset of GFP-expressing cells in the periglomeruli of the olfactory bulb did not express GFAP immunoreactivity. Collectively, these results suggest that human GFAP promoter-derived GFP expression does not faithfully recapitulate the endogenous GFAP expression in mice, suggesting that upstream regulatory mechanisms controlling GFAP transcription are different in different populations of astrocytes, and may reflect the functional diversity of astrocytes.

Keywords

References

  1. Araque A, Navarrete M. 2010. Glial cells in neuronal network function. Phil Trans R Soc of Lond B. 365:2375-2381. https://doi.org/10.1098/rstb.2009.0313
  2. Bahjaoui-Bouhaddi M, Padilla F, Nicolet M, Cifuentes-Diaz C, Fellmann D, Mege RM. 1997. Localized deposition of M-cadherin in the glomeruli of the granular layer during the postnatal development of mouse cerebellum. J Comp Neurol. 378:180-195. https://doi.org/10.1002/(SICI)1096-9861(19970210)378:2<180::AID-CNE3>3.0.CO;2-#
  3. Bailey MS, Shipley MT. 1993. Astrocyte subtypes in the rat olfactory bulb: morphological heterogeneity and differential laminar distribution. J Comp Neurol. 328:501-526. https://doi.org/10.1002/cne.903280405
  4. Bonfanti L, Peretto P. 2007. Radial glial origin of the adult neural stem cells in the subventricular zone. Prog Neurobiol. 83:24-36. https://doi.org/10.1016/j.pneurobio.2006.11.002
  5. Bordey A, Sontheimer H. 2000. Ion channel expression by astrocytes in situ: comparison of different CNS regions. Glia. 30:27-38. https://doi.org/10.1002/(SICI)1098-1136(200003)30:1<27::AID-GLIA4>3.0.CO;2-#
  6. Brenner M, Kisseberth WC, Su Y, Besnard F, Messing A. 1994. GFAP promoter directs astrocyte-specific expression in transgenic mice. J Neurosci. 14:1030-1037.
  7. Brunne B, Zhao S, Derouiche A, Herz J, May P, Frotscher M, Bock HH. 2010. Origin, maturation, and astroglial transformation of secondary radial glial cells in the developing dentate gyrus. Glia. 58:1553-1569.
  8. Casper KB, McCarthy KD. 2006. GFAP-positive progenitor cells produce neurons and oligodendrocytes throughout the CNS. Mol Cell Neurosci. 31:676-684. https://doi.org/10.1016/j.mcn.2005.12.006
  9. Chu Y, Hughes S, Chan-Ling T. 2001. Differentiation and migration of astrocyte precursor cells and astrocytes in human fetal retina: relevance to optic nerve coloboma. Faseb J. 15:2013-2015. https://doi.org/10.1096/fj.00-0868fje
  10. Eckenhoff MF, Rakic P. 1984. Radial organization of the hippocampal dentate gyrus: a Golgi, ultrastructural, and immunocytochemical analysis in the developing rhesus monkey. J Comp Neurol. 223:1-21. https://doi.org/10.1002/cne.902230102
  11. Emsley JG, Arlotta P, Macklis JD. 2004. Star-cross'd neurons: astroglial effects on neural repair in the adult mammalian CNS. Trends Neurosci. 27:238-240. https://doi.org/10.1016/j.tins.2004.02.008
  12. Eng LF, Ghirnikar RS, Lee YL. 2000. Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000). Neurochem Res. 25:1439-1451. https://doi.org/10.1023/A:1007677003387
  13. Frotscher M, Zhao S, Forster E. 2007. Development of cell and fiber layers in the dentate gyrus. Prog Brain Res. 163:133-142.
  14. Ganat YM, Silbereis J, Cave C, Ngu H, Anderson GM, Ohkubo Y, Ment LR, Vaccarino FM. 2006. Early postnatal astroglial cells produce multilineage precursors and neural stem cells in vivo. J Neurosci. 26:8609-8621. https://doi.org/10.1523/JNEUROSCI.2532-06.2006
  15. Garcia AD, Doan NB, Imura T, Bush TG, Sofroniew MV. 2004. GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci. 7:1233-1241. https://doi.org/10.1038/nn1340
  16. Gressens P, Evrard P. 1993. The glial fascicle: an ontogenic and phylogenic unit guiding, supplying and distributing mammalian cortical neurons. Brain Res Dev Brain Res. 76:272-277. https://doi.org/10.1016/0165-3806(93)90218-Y
  17. Hatten ME. 1999. Central nervous system neuronal migration. Annu Rev Neurosci. 22:511-539. https://doi.org/10.1146/annurev.neuro.22.1.511
  18. Hill SJ, Barbarese E, McIntosh TK. 1996. Regional heterogeneity in the response of astrocytes following traumatic brain injury in the adult rat. J Neuropathol Exp Neurol. 55:1221-1229. https://doi.org/10.1097/00005072-199612000-00005
  19. Jabs R, Pivneva T, Huttmann K, Wyczynski A, Nolte C, Kettenmann H, Steinhauser C. 2005. Synaptic transmission onto hippocampal glial cells with hGFAP promoter activity. J Cell Sci 118:3791-3803. https://doi.org/10.1242/jcs.02515
  20. Kim WR, Kim Y, Eun B, Park OH, Kim H, Kim K, Park CH, Vinsant S, Oppenheim RW, Sun W. 2007. Impaired migration in the rostral migratory stream but spared olfactory function after the elimination of programmed cell death in Bax knock-out mice. J Neurosci. 27:14392-14403. https://doi.org/10.1523/JNEUROSCI.3903-07.2007
  21. Kim SE, Ko IG, Kim BK, Sung YH, Shin MS, Cho S, Kim CJ, Kim KH, Lee KW, Kim DH. 2010. Transplantation of human adipose-derived stem cells into the urethra ameliorates stress urinary incontinence and blunts the induction of c-Fos immunoreactivities in brain areas related to micturition in female rats. Anim Cells Syst. 14:237-244. https://doi.org/10.1080/19768354.2010.525839
  22. Kimelberg HK. 2004. The problem of astrocyte identity. Neurochem Int. 45:191-202. https://doi.org/10.1016/j.neuint.2003.08.015
  23. Kondo Y, Ogawa N, Asanuma M, Ota Z, Mori A. 1995. Regional differences in late-onset iron deposition, ferritin, transferrin, astrocyte proliferation, and microglial activation after transient forebrain ischemia in rat brain. J Cereb Blood Flow Metab. 15:216-226. https://doi.org/10.1038/jcbfm.1995.27
  24. Kriegstein AR, Gotz M. 2003. Radial glia diversity: a matter of cell fate. Glia. 43:37-43. https://doi.org/10.1002/glia.10250
  25. Kuhn HG, Dickinson-Anson H, Gage FH. 1996. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci. 16:2027-2033.
  26. Lafarga M, Berciano MT, Saurez I, Andres MA, Berciano J. 1993. Reactive astroglia-neuron relationships in the human cerebellar cortex: a quantitative, morphological and immunocytochemical study in Creutzfeldt-Jakob disease. Int J Dev Neurosci. 11:199-213. https://doi.org/10.1016/0736-5748(93)90079-S
  27. Lee Y, Su M, Messing A, Brenner M. 2006. Astrocyte heterogeneity revealed by expression of a GFAP-LacZ transgene. Glia. 53:677-687. https://doi.org/10.1002/glia.20320
  28. Lee Y, Messing A, Su M, Brenner M. 2008. GFAP promoter elements required for region-specific and astrocytespecific expression. Glia. 56:481-493. https://doi.org/10.1002/glia.20622
  29. Liu X, Bolteus AJ, Balkin DM, Henschel O, Bordey A. 2006. GFAP-expressing cells in the postnatal subventricular zone display a unique glial phenotype intermediate between radial glia and astrocytes. Glia. 54:394-410. https://doi.org/10.1002/glia.20392
  30. Matthias K, Kirchhoff F, Seifert G, Huttmann K, Matyash M, Kettenmann H, Steinhauser C. 2003. Segregated expression of AMPA-type glutamate receptors and glutamate transporters defines distinct astrocyte populations in the mouse hippocampus. J Neurosci. 23:1750- 1758.
  31. Morga E, Faber C, Heuschling P. 1999. Regional heterogeneity of the astroglial immunoreactive phenotype: effect of lipopolysaccharide. J Neurosci Res. 57:941-952. https://doi.org/10.1002/(SICI)1097-4547(19990915)57:6<941::AID-JNR20>3.0.CO;2-Z
  32. Nolte C, Matyash M, Pivneva T, Schipke CG, Ohlemeyer C, Hanisch UK, Kirchhoff F, Kettenmann H. 2001. GFAP promoter-controlled EGFP-expressing transgenic mice: a tool to visualize astrocytes and astrogliosis in living brain tissue. Glia. 33:72-86. https://doi.org/10.1002/1098-1136(20010101)33:1<72::AID-GLIA1007>3.0.CO;2-A
  33. Ogata K, Kosaka T. 2002. Structural and quantitative analysis of astrocytes in the mouse hippocampus. Neuroscience. 113:221-233. https://doi.org/10.1016/S0306-4522(02)00041-6
  34. Pixley SK, de Vellis J. 1984. Transition between immature radial glia and mature astrocytes studied with a monoclonal antibody to vimentin. Brain Res. 317:201-209.
  35. Platel JC, Gordon V, Heintz T, Bordey A. 2009. GFAP-GFP neural progenitors are antigenically homogeneous and anchored in their enclosed mosaic niche. Glia. 57:66-78. https://doi.org/10.1002/glia.20735
  36. Rakic P. 2003. Elusive radial glial cells: historical and evolutionary perspective. Glia. 43:19-32. https://doi.org/10.1002/glia.10244
  37. Reyher CK, Lubke J, Larsen WJ, Hendrix GM, Shipley MT, Baumgarten HG. 1991. Olfactory bulb granule cell aggregates: morphological evidence for interperikaryal electrotonic coupling via gap junctions. J Neurosci. 11:1485-1495.
  38. Ruzicka BB, Fox CA, Thompson RC, Meng F, Watson SJ, Akil H. 1995. Primary astroglial cultures derived from several rat brain regions differentially express mu, delta and kappa opioid receptor mRNA. Brain Res Mol Brain Res. 34:209-2208. https://doi.org/10.1016/0169-328X(95)00165-O
  39. Seri B, Garcia-Verdugo JM, Collado-Morente L, McEwen BS, Alvarez-Buylla A. 2004. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol. 478:359-378. https://doi.org/10.1002/cne.20288
  40. Silbereis J, Heintz T, Taylor MM, Ganat Y, Ment LR, Bordey A, Vaccarino F. 2010. Astroglial cells in the external granular layer are precursors of cerebellar granule neurons in neonates. Mol Cell Neurosci. 44:362-373. https://doi.org/10.1016/j.mcn.2010.05.001
  41. Sontheimer H. 1992. Astrocytes, as well as neurons, express a diversity of ion channels. Can J Physiol Pharmacol. 70(Suppl):S223-238. https://doi.org/10.1139/y92-266
  42. Su M, Hu H, Lee Y, d'Azzo A, Messing A, Brenner M. 2004. Expression specificity of GFAP transgenes. Neurochem Res. 29:2075-2093. https://doi.org/10.1007/s11064-004-6881-1
  43. Suhonen JO, Peterson DA, Ray J, Gage FH. 1996. Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo. Nature. 383:624-627. https://doi.org/10.1038/383624a0
  44. Tramontin AD, Garcia-Verdugo JM, Lim DA, Alvarez- Buylla A. 2003. Postnatal development of radial glia and the ventricular zone (VZ): a continuum of the neural stem cell compartment. Cereb Cortex. 13:580-587. https://doi.org/10.1093/cercor/13.6.580
  45. Yamada H, Fredette B, Shitara K, Hagihara K, Miura R, Ranscht B, Stallcup WB, Yamaguchi Y. 1997. The brain chondroitin sulfate proteoglycan brevican associates with astrocytes ensheathing cerebellar glomeruli and inhibits neurite outgrowth from granule neurons. J Neuroscience. 17:7784-7795.
  46. Zerlin M, Milosevic A, Goldman JE. 2004. Glial progenitors of the neonatal subventricular zone differentiate asynchronously, leading to spatial dispersion of glial clones and to the persistence of immature glia in the adult mammalian CNS. Dev Biol. 270:200-213. https://doi.org/10.1016/j.ydbio.2004.02.024
  47. Zhang SC. 2001. Defining glial cells during CNS development. Nat Rev Neurosci 2:840-843. https://doi.org/10.1038/35097593
  48. Zhuo L, Sun B, Zhang CL, Fine A, Chiu SY, Messing A. 1997. Live astrocytes visualized by green fluorescent protein in transgenic mice. Dev Biol. 187:36-42. https://doi.org/10.1006/dbio.1997.8601

Cited by

  1. Expression of ezrin in subventricular zone neural stem cells and their progeny in adult and developing mice vol.139, pp.3, 2011, https://doi.org/10.1007/s00418-012-1048-7
  2. Finding degrees of separation: Experimental approaches for astroglial and oligodendroglial cell isolation and genetic targeting vol.236, pp.None, 2011, https://doi.org/10.1016/j.jneumeth.2014.08.017
  3. Astrocyte IKKβ/NF-κB signaling is required for diet-induced obesity and hypothalamic inflammation vol.6, pp.4, 2011, https://doi.org/10.1016/j.molmet.2017.01.010
  4. Exposure to Arsenic Alters the Microbiome of Larval Zebrafish vol.9, pp.None, 2011, https://doi.org/10.3389/fmicb.2018.01323