Anatomy and Cell Biology

Korean Association of Anatomists (대한해부학회)
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ID4 mediates proliferation of astrocytes after excitotoxic damage in the mouse hippocampus

  • Lee, Young-Sook (Department of Anatomy, School of Medicine, Chungnam National University) ;
  • Kang, Joon-Won (Department of Pediatrics, School of Medicine, Chungnam National University) ;
  • Lee, Young-Ho (Department of Anatomy, School of Medicine, Chungnam National University) ;
  • Kim, Dong-Woon (Department of Anatomy, School of Medicine, Chungnam National University)
  • Published : 2011.06.30
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Abstract

Inhibitor of DNA binding (ID) proteins bind to and inhibit the function of basic helix-loop-helix transcription factors, including those that regulate proliferation and differentiation during development. However, little is known about the role of ID proteins in glial activation under neuropathological conditions. In this study, we evaluated the expression of ID4 following induction of excitotoxic lesions in mouse brain by kainic acid injection. The number of ID4-expressing astrocytes increased in the CA1 layer of the injured hippocampus until 3 days post-lesion. To analyze the effects of ID4 on cell proliferation, primary astrocytes were transduced with recombinant adenovirus expressing GFP-ID4. Overexpression of ID4 led to increased proliferation of astrocytes. These results suggest that ID4 plays a proliferative role in astrocyte activation after excitotoxin-induced hippocampal neuronal death.

Keywords

References

  1. de Candia P, Benera R, Solit DB. A role for Id proteins in mammary gland physiology and tumorigenesis. Adv Cancer Res 2004;92:81-94.
  2. Perk J, Iavarone A, Benezra R. Id family of helix-loop-helix proteins in cancer. Nat Rev Cancer 2005;5:603-14. https://doi.org/10.1038/nrc1673
  3. Norton JD. ID helix-loop-helix proteins in cell growth, differentiation and tumorigenesis. J Cell Sci 2000;113(Pt 22):3897-905.
  4. Andres-Barquin PJ, Hernandez MC, Israel MA. Id genes in nervous system development. Histol Histopathol 2000;15:603-18.
  5. Jen Y, Manova K, Benezra R. Each member of the Id gene family exhibits a unique expression pattern in mouse gastrulation and neurogenesis. Dev Dyn 1997;208:92-106. https://doi.org/10.1002/(SICI)1097-0177(199701)208:1<92::AID-AJA9>3.0.CO;2-X
  6. Riechmann V, Sablitzky F. Mutually exclusive expression of two dominant-negative helix-loop-helix (dnHLH) genes, Id4 and Id3, in the developing brain of the mouse suggests distinct regulatory roles of these dnHLH proteins during cellular proliferation and differentiation of the nervous system. Cell Growth Differ 1995;6:837-43.
  7. Andres-Barquin PJ, Hernandez MC, Israel MA. Id4 expression induces apoptosis in astrocytic cultures and is down-regulated by activation of the cAMP-dependent signal transduction pathway. Exp Cell Res 1999;247:347-55. https://doi.org/10.1006/excr.1998.4360
  8. van Cruchten I, Cinato E, Fox M, King ER, Newton JS, Riechmann V, Sablitzky F. Structure, chromosomal localisation and expression of the murine dominant negative helix-loophelix Id4 gene. Biochim Biophys Acta 1998;1443:55-64. https://doi.org/10.1016/S0167-4781(98)00196-1
  9. Kondo T, Raff M. The Id4 HLH protein and the timing of oligodendrocyte differentiation. EMBO J 2000;19:1998-2007. https://doi.org/10.1093/emboj/19.9.1998
  10. Liang Y, Bollen AW, Nicholas MK, Gupta N. Id4 and FABP7 are preferentially expressed in cells with astrocytic features in oligodendrogliomas and oligoastrocytomas. BMC Clin Pathol 2005;5:6. https://doi.org/10.1186/1472-6890-5-6
  11. Jeon HM, Jin X, Lee JS, Oh SY, Sohn YW, Park HJ, Joo KM, Park WY, Nam DH, DePinho RA, Chin L, Kim H. Inhibitor of differentiation 4 drives brain tumor-initiating cell genesis through cyclin E and notch signaling. Genes Dev 2008;22:2028-33. https://doi.org/10.1101/gad.1668708
  12. Nadler JV, Perry BW, Gentry C, Cotman CW. Degeneration of hippocampal CA3 pyramidal cells induced by intraventricular kainic acid. J Comp Neurol 1980;192:333-59. https://doi.org/10.1002/cne.901920209
  13. Kim DW, Lee JH, Park SK, Yang WM, Jeon GS, Lee YH, Chung CK, Cho SS. Astrocytic expressions of phosphorylated Akt, GSK3beta and CREB following an excitotoxic lesion in the mouse hippocampus. Neurochem Res 2007;32:1460-8. https://doi.org/10.1007/s11064-007-9332-y
  14. Laursen SE, Belknap JK. Intracerebroventricular injections in mice. Some methodological refinements. J Pharmacol Methods 1986;16:355-7. https://doi.org/10.1016/0160-5402(86)90038-0
  15. Luna-Medina R, Cortes-Canteli M, Alonso M, Santos A, Martinez A, Perez-Castillo A. Regulation of inflammatory response in neural cells in vitro by thiadiazolidinones derivatives through peroxisome proliferator-activated receptor gamma activation. J Biol Chem 2005;280:21453-62. https://doi.org/10.1074/jbc.M414390200
  16. Lee YS, Mollah ML, Sohn KC, Shi G, Kim DH, Kim KH, Cho MJ, Kim S, Lee YH, Kim CD, Lee JH. ID3 mediates X-rayinduced apoptosis of keratinocytes through the regulation of beta-catenin. J Dermatol Sci 2010;60:138-42. https://doi.org/10.1016/j.jdermsci.2010.09.002
  17. Lee YS, Sohn KC, Jang S, Lee Y, Hwang C, Kim KH, Cho MJ, Kim CD, Lee JH. Anti-apoptotic role of S100A8 in X-ray irradiated keratinocytes. J Dermatol Sci 2008;51:11-8. https://doi.org/10.1016/j.jdermsci.2008.01.003
  18. Cho IH, Hong J, Suh EC, Kim JH, Lee H, Lee JE, Lee S, Kim CH, Kim DW, Jo EK, Lee KE, Karin M, Lee SJ. Role of microglial IKKbeta in kainic acid-induced hippocampal neuronal cell death. Brain 2008;131(Pt 11):3019-33. https://doi.org/10.1093/brain/awn230
  19. Bedford L, Walker R, Kondo T, van Cruchten I, King ER, Sablitzky F. Id4 is required for the correct timing of neural differentiation. Dev Biol 2005;280:386-95. https://doi.org/10.1016/j.ydbio.2005.02.001
  20. Yun K, Mantani A, Garel S, Rubenstein J, Israel MA. Id4 regulates neural progenitor proliferation and differentiation in vivo. Development 2004;131:5441-8. https://doi.org/10.1242/dev.01430
  21. Murad JM, Place CS, Ran C, Hekmatyar SK, Watson NP, Kauppinen RA, Israel MA. Inhibitor of DNA binding 4 (ID4) regulation of adipocyte differentiation and adipose tissue formation in mice. J Biol Chem 2010;285:24164-73. https://doi.org/10.1074/jbc.M110.128744
  22. Du Y, Yip HK. The expression and roles of inhibitor of DNA binding helix-loop-helix proteins in the developing and adult mouse retina. Neuroscience 2011;175:367-79. https://doi.org/10.1016/j.neuroscience.2010.12.007
  23. Fontemaggi G, Dell'Orso S, Trisciuoglio D, Shay T, Melucci E, Fazi F, Terrenato I, Mottolese M, Muti P, Domany E, Del Bufalo D, Strano S, Blandino G. The execution of the transcriptional axis mutant p53, E2F1 and ID4 promotes tumor neo-angiogenesis. Nat Struct Mol Biol 2009;16:1086-93. https://doi.org/10.1038/nsmb.1669
  24. Kuzontkoski PM, Mulligan-Kehoe MJ, Harris BT, Israel MA. Inhibitor of DNA binding-4 promotes angiogenesis and growth of glioblastoma multiforme by elevating matrix GLA levels. Oncogene 2010;29:3793-802. https://doi.org/10.1038/onc.2010.147
  25. Altman J. Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 1969;137:433-57. https://doi.org/10.1002/cne.901370404
  26. Ninomiya M, Yamashita T, Araki N, Okano H, Sawamoto K. Enhanced neurogenesis in the ischemic striatum following EGF-induced expansion of transit-amplifying cells in the subventricular zone. Neurosci Lett 2006;403:63-7. https://doi.org/10.1016/j.neulet.2006.04.039
  27. Nakatomi H, Kuriu T, Okabe S, Yamamoto S, Hatano O, Kawahara N, Tamura A, Kirino T, Nakafuku M. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 2002;110:429-41. https://doi.org/10.1016/S0092-8674(02)00862-0
  28. Parent JM, von dem Bussche N, Lowenstein DH. Prolonged seizures recruit caudal subventricular zone glial progenitors into the injured hippocampus. Hippocampus 2006;16:321-8. https://doi.org/10.1002/hipo.20166
  29. Shetty AK. Entorhinal axons exhibit sprouting in CA1 subfield of the adult hippocampus in a rat model of temporal lobe epilepsy. Hippocampus 2002;12:534-42. https://doi.org/10.1002/hipo.10031

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