Heterozygous modulation of TGF-β signaling does not influence Müller glia cell reactivity or proliferation following NMDA-induced damage

Histochemistry and Cell Biology

Volumn 144, Issue 5, 2015, Pages 443-455

  Kugler, Martina ^a   Schlecht, Anja ^a   Fuchshofer, Rudolf ^a   Kleiter, Ingo ^b   Aigner, Ludwig ^c   Tamm, Ernst R ^a   Braunger, Barbara M ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b ST JOSEF HOSPITAL   (Germany)

^c PARACELSUS MEDICAL UNIVERSITY   (Austria)

Author keywords

M ller glia cells; NMDA; Proliferation; Regeneration; Stem cells; TGF signaling

Indexed keywords

BROXURIDINE; GENOMIC DNA; GLIAL FIBRILLARY ACIDIC PROTEIN; N METHYL DEXTRO ASPARTIC ACID; NESTIN; RNA; SMAD7 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; N METHYLASPARTIC ACID;

ADULT; ADULT STEM CELL; ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DAMAGE; CELL PROLIFERATION; CELL TRANSDIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EXCITOTOXICITY; GENOTYPE; GLIA CELL; HETEROZYGOTE; IMMUNOHISTOCHEMISTRY; MOUSE; MUELLER CELL; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RETINA AMACRINE CELL; RETINA GANGLION CELL; RETINA NERVE CELL; RETINA NEUROEPITHELIAL LAYER; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; ANIMAL; DRUG EFFECTS; GLIA; INTRAVITREAL DRUG ADMINISTRATION; METABOLISM;

ANIMALS; CELL PROLIFERATION; INTRAVITREAL INJECTIONS; MICE; N-METHYLASPARTATE; NEUROGLIA; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84945492707     PISSN: 09486143     EISSN: 1432119X     Source Type: Journal    
DOI: 10.1007/s00418-015-1354-y     Document Type: Article

References (52)

1. Alberts B, Johnson A, Lewis J et al (2002) Molecular biology of the cell. http://www.ncbi.nlm.nih.gov/books/NBK21054/. Accessed 26 Mar 2014
2. Bernardos RL, Barthel LK, Meyers JR, Raymond PA (2007) Late-stage neuronal progenitors in the retina are radial Müller glia that function as retinal stem cells. J Neurosci Off J Soc Neurosci 27:7028–7040. doi:10.1523/JNEUROSCI.1624-07.2007
3. Brahmachari S, Fung YK, Pahan K (2006) Induction of glial fibrillary acidic protein expression in astrocytes by nitric oxide. J Neurosci 26:4930–4939. doi:10.1523/JNEUROSCI.5480-05.2006
4. Braisted JE, Essman TF, Raymond PA (1994) Selective regeneration of photoreceptors in goldfish retina. Dev Camb Engl 120:2409–2419
5. Braunger BM, Ohlmann A, Koch M et al (2013a) Constitutive overexpression of Norrin activates Wnt/β-catenin and endothelin-2 signaling to protect photoreceptors from light damage. Neurobiol Dis 50:1–12. doi:10.1016/j.nbd.2012.09.008
6. Braunger BM, Pielmeier S, Demmer C et al (2013b) TGF-β Signaling Protects Retinal Neurons from Programmed Cell Death during the Development of the Mammalian Eye. J Neurosci 33:14246–14258. doi:10.1523/JNEUROSCI.0991-13.2013
7. Bringmann A, Reichenbach A (2001) Role of Muller cells in retinal degenerations. Front Biosci J Virtual Libr 6:E72–E92
8. Bringmann A, Pannicke T, Grosche J et al (2006) Müller cells in the healthy and diseased retina. Prog Retin Eye Res 25:397–424. doi:10.1016/j.preteyeres.2006.05.003
9. Chen Q, Chen H, Zheng D et al (2009) Smad7 is required for the development and function of the heart. J Biol Chem 284:292–300. doi:10.1074/jbc.M807233200
10. Chytil A, Magnuson MA, Wright CVE, Moses HL (2002) Conditional inactivation of the TGF-beta type II receptor using Cre:Lox. Genesis 32:73–75
11. Close JL, Gumuscu B, Reh TA (2005) Retinal neurons regulate proliferation of postnatal progenitors and Müller glia in the rat retina via TGF beta signaling. Dev Camb Engl 132:3015–3026. doi:10.1242/dev.01882
12. Cotsarelis G, Cheng SZ, Dong G et al (1989) Existence of slow-cycling limbal epithelial basal cells that can be preferentially stimulated to proliferate: implications on epithelial stem cells. Cell 57:201–209
13. Dyer MA, Cepko CL (2000) Control of Müller glial cell proliferation and activation following retinal injury. Nat Neurosci 3:873–880. doi:10.1038/78774
14. Ema H, Suda T (2012) Two anatomically distinct niches regulate stem cell activity. Blood 120:2174–2181. doi:10.1182/blood-2012-04-424507
15. Fischer AJ (2005) Neural regeneration in the chick retina. Prog Retin Eye Res 24:161–182. doi:10.1016/j.preteyeres.2004.07.003
16. Fischer AJ, Reh TA (2002) Exogenous growth factors stimulate the regeneration of ganglion cells in the chicken retina. Dev Biol 251:367–379
17. Forrester E, Chytil A, Bierie B et al (2005) Effect of conditional knockout of the type II TGF-beta receptor gene in mammary epithelia on mammary gland development and polyomavirus middle T antigen induced tumor formation and metastasis. Cancer Res 65:2296–2302. doi:10.1158/0008-5472.CAN-04-3272
18. Frisén J, Johansson CB, Török C et al (1995) Rapid, widespread, and longlasting induction of nestin contributes to the generation of glial scar tissue after CNS injury. J Cell Biol 131:453–464
19. García M, Vecino E (2003) Role of Müller glia in neuroprotection and regeneration in the retina. Histol Histopathol 18:1205–1218
20. Helgadóttir G, Jónasson F, Sigurdsson H et al (2006) Age related macular degeneration. Læknablađiđ 92:685–696
21. Hitchcock P, Ochocinska M, Sieh A, Otteson D (2004) Persistent and injury-induced neurogenesis in the vertebrate retina. Prog Retin Eye Res 23:183–194. doi:10.1016/j.preteyeres.2004.01.001
22. Ikeda T, Homma Y, Nisida K et al (1998) Expression of transforming growth factor-beta s and their receptors by human retinal glial cells. Curr Eye Res 17:546–550
23. Inamoto S, Kwartler CS, Lafont AL et al (2010) TGFBR2 mutations alter smooth muscle cell phenotype and predispose to thoracic aortic aneurysms and dissections. Cardiovasc Res 88:520–529. doi:10.1093/cvr/cvq230
24. Joly S, Pernet V, Samardzija M, Grimm C (2011) Pax6-positive Müller glia cells express cell cycle markers but do not proliferate after photoreceptor injury in the mouse retina. Glia 59:1033–1046. doi:10.1002/glia.21174
25. Kandasamy M, Couillard-Despres S, Raber KA et al (2010) Stem cell quiescence in the hippocampal neurogenic niche is associated with elevated transforming growth factor-beta signaling in an animal model of Huntington disease. J Neuropathol Exp Neurol 69:717–728. doi:10.1097/NEN.0b013e3181e4f733
26. Kandasamy M, Reilmann R, Winkler J et al (2011) Transforming growth factor-beta signaling in the neural stem cell niche: a therapeutic target for Huntington’s disease. Neurol Res Int 2011:124256. doi:10.1155/2011/124256
27. Karl MO, Hayes S, Nelson BR et al (2008) Stimulation of neural regeneration in the mouse retina. Proc Natl Acad Sci 105:19508–19513. doi:10.1073/pnas.0807453105
28. Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137–138
29. Kettenmann H, Ransom BR (2005) Neuroglia. Oxford University Press, Oxford
30. Kleiter I, Song J, Lukas D et al (2010) Smad7 in T cells drives T helper 1 responses in multiple sclerosis and experimental autoimmune encephalomyelitis. Brain J Neurol 133:1067–1081. doi:10.1093/brain/awq039
31. Lakso M, Pichel JG, Gorman JR et al (1996) Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc Natl Acad Sci USA 93:5860–5865
32. Lenkowski JR, Qin Z, Sifuentes CJ et al (2013) Retinal regeneration in adult zebrafish requires regulation of TGFβ signaling. Glia 61:1687–1697. doi:10.1002/glia.22549
33. Levéen P, Larsson J, Ehinger M et al (2002) Induced disruption of the transforming growth factor beta type II receptor gene in mice causes a lethal inflammatory disorder that is transplantable. Blood 100:560–568
34. Loeys BL, Chen J, Neptune ER et al (2005) A syndrome of altered cardiovascular, craniofacial, neurocognitive and skeletal development caused by mutations in TGFBR1 or TGFBR2. Nat Genet 37:275–281. doi:10.1038/ng1511
35. Massagué J (1998) TGF-beta signal transduction. Annu Rev Biochem 67:753–791. doi:10.1146/annurev.biochem.67.1.753
36. Mizuguchi T, Collod-Beroud G, Akiyama T et al (2004) Heterozygous TGFBR2 mutations in Marfan syndrome. Nat Genet 36:855–860. doi:10.1038/ng1392
37. Mori T, Tanaka K, Buffo A et al (2006) Inducible gene deletion in astroglia and radial glia—a valuable tool for functional and lineage analysis. Glia 54:21–34. doi:10.1002/glia.20350
38. Moshiri A, Close J, Reh TA (2004) Retinal stem cells and regeneration. Int J Dev Biol 48:1003–1014. doi:10.1387/ijdb.041870am
39. Oshima M, Oshima H, Taketo MM (1996) TGF-beta receptor type II deficiency results in defects of yolk sac hematopoiesis and vasculogenesis. Dev Biol 179:297–302. doi:10.1006/dbio.1996.0259
40. Raymond PA, Hitchcock PF (2000) How the neural retina regenerates. Results Probl Cell Differ 31:197–218
41. Raymond PA, Barthel LK, Bernardos RL, Perkowski JJ (2006) Molecular characterization of retinal stem cells and their niches in adult zebrafish. BMC Dev Biol 6:36. doi:10.1186/1471-213X-6-36
42. Richardson KC, Jarett L, Finke EH (1960) Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol 35:313–323
43. Seitz R, Hackl S, Seibuchner T et al (2010) Norrin mediates neuroprotective effects on retinal ganglion cells via activation of the Wnt/beta-catenin signaling pathway and the induction of neuroprotective growth factors in Muller cells. J Neurosci 30:5998–6010. doi:10.1523/JNEUROSCI.0730-10.2010
44. Tackenberg MA, Tucker BA, Swift JS et al (2009) Müller cell activation, proliferation and migration following laser injury. Mol Vis 15:1886–1896
45. Tojo M, Takebe A, Takahashi S et al (2012) Smad7-deficient mice show growth retardation with reduced viability. J Biochem (Tokyo) 151:621–631. doi:10.1093/jb/mvs022
46. Ueki Y, Reh TA (2013) EGF stimulates Müller glial proliferation via a BMP-dependent mechanism. Glia 61:778–789. doi:10.1002/glia.22472
47. Varma R, Peeples P, Walt JG, Bramley TJ (2008) Disease progression and the need for neuroprotection in glaucoma management. Am J Manag Care 14:S15–S19
48. Vihtelic TS, Hyde DR (2000) Light-induced rod and cone cell death and regeneration in the adult albino zebrafish (Danio rerio) retina. J Neurobiol 44:289–307
49. Visser JA, Themmen AP (1998) Downstream factors in transforming growth factor-β family signaling. Mol Cell Endocrinol 146:7–17. doi:10.1016/S0303-7207(98)00198-1
50. Voog J, Jones DL (2010) Stem cells and the niche: a dynamic duo. Cell Stem Cell 6:103–115. doi:10.1016/j.stem.2010.01.011
51. Wachs F-P, Winner B, Couillard-Despres S et al (2006) Transforming growth factor-beta1 is a negative modulator of adult neurogenesis. J Neuropathol Exp Neurol 65:358–370. doi:10.1097/01.jnen.0000218444.53405.f0
52. Wang Y, Rattner A, Zhou Y et al (2012) Norrin/Frizzled4 signaling in retinal vascular development and blood brain barrier plasticity. Cell 151:1332–1344. doi:10.1016/j.cell.2012.10.042