Anatomy and Cell Biology

Korean Association of Anatomists (대한해부학회)
권호 표지
DOI QR코드

DOI QR Code

Expression of ErbB4 in the apoptotic neurons of Alzheimer's disease brain

  • Woo, Ran-Sook (Department of Anatomy and Neuroscience, College of Medicine, Eulji University) ;
  • Lee, Ji-Hye (Department of Anatomy and Neuroscience, College of Medicine, Eulji University) ;
  • Yu, Ha-Nul (Department of Anatomy and Neuroscience, College of Medicine, Eulji University) ;
  • Song, Dae-Yong (Department of Anatomy and Neuroscience, College of Medicine, Eulji University) ;
  • Baik, Tai-Kyoung (Department of Anatomy and Neuroscience, College of Medicine, Eulji University)
  • Received : 2010.10.18
  • Accepted : 2010.11.09
  • Published : 2010.12.30
⟨ Previous Next ⟩

Abstract

Neuregulin-1 (NRG1) signaling participates in the synaptic plasticity, maintenance or regulation of adult brain. Although ErbB4, a key NRG1 receptor, is expressed in multiple regions in the adult animal brain, little is known about its localization in Alzheimer’s disease (AD) brains. We previously reported that ErbB4 immunoreactivity showed regional difference in the hippocampus of age-matched control. In the present paper, immunohistochemical characterization of the distribution of ErbB4 receptor in the hippocampus relative to pathology staging were performed in age-matched control (Braak stage 0, n=6) and AD (Braak stage I/V, n=10). Here, we found that ErbB4 immunoreactivity was significantly increased in apoptotic hippocampal pyramidal neurons in the brains of AD patients, compared to those of age-matched control subjects. In AD brains, ErbB4 immunoreactivity was demonstrated to colocalize with the apoptotic signal Bax in apoptotic hippocampal pyramidal neurons. These results suggest that up-regulation of ErbB4 immunoreactivity in apoptotic neuron may involve in the progression of pathology of AD.

Keywords

Acknowledgement

Grant : Korea Healthcare technology R&D Project

Supported by : Ministry for Health, Welfare and Family Affairs, Republic of Korea

References

  1. Braak H, Braak E. (1991). Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82: 239-259 https://doi.org/10.1007/BF00308809
  2. Campbell SK, Switzer RC, Martin TL. (1987). Alzheimers plaques and tangles: a controled and enhanced silver staining method. In Proceeding Soc Neurosci 678
  3. Chaudhury AR, Gerecke KM, Wyss JM, Morgan DG, Gordon MN, Carroll SL. (2003). Neuregulin-1 and erbB4 immunoreactivity is associated with neuritic plaques in Alzheimer disease brain and in a transgenic model of Alzheimer disease. J Neuropathol Exp Neurol 62: 42-54 https://doi.org/10.1093/jnen/62.1.42
  4. Clementi ME, Pezzotti M, Orsini F, et al. (2006). Alzheimer's amyloid beta-peptide (1-42) induces cell death in human neuroblastoma via bax/bcl-2 ratio increase: an intriguing role for methionine 35. Biochem Biophys Res Commun 342: 206-213 https://doi.org/10.1016/j.bbrc.2006.01.137
  5. Croslan DR, Schoell MC, Ford GD, et al. (2008). Neuroprotective effects of neuregulin-1 on B35 neuronal cells following ischemia. Brain Res 1210: 39-47 https://doi.org/10.1016/j.brainres.2008.02.059
  6. Cutler RG, Kelly J, Storie K, et al. (2004). Involvement of oxidative stress-induced abnormalities in ceramide and cholesterol metabolism in brain aging and Alzheimer's disease. Proc Natl Acad Sci USA 101: 2070-2075 https://doi.org/10.1073/pnas.0305799101
  7. Di Segni A, Shaharabani E, Stein R, Pinkas-Kramarski R. (2005). Neuregulins rescue PC12-ErbB-4 cells from cell death induced by beta-amyloid peptide: involvement of PI3K and PKC. J Mol Neurosci 26: 57-69 https://doi.org/10.1385/JMN:26:1:057
  8. Ezaki T. (2000). Antigen retrieval on formaldehyde-fixed paraffin sections: its potential drawbacks and optimization for double immunostaining. Micron 31: 639-649 https://doi.org/10.1016/S0968-4328(99)00064-5
  9. Garcia RA, Vasudevan K, Buonanno A. (2000). The neuregulin receptor ErbB-4 interacts with PDZ-containing proteins at neuronal synapses. Proc Natl Acad Sci U S A 97: 3596-3601 https://doi.org/10.1073/pnas.070042497
  10. Goldshmit Y, Erlich S, Pinkas-Kramarski R. (2001). Neuregulin rescues PC12-ErbB4 cells from cell death induced by H(2)O(2). Regulation of reactive oxygen species levels by phosphatidylinositol 3-kinase. J Biol Chem 276: 46379-46385 https://doi.org/10.1074/jbc.M105637200
  11. Gonatas NK, Anderson W, Evangelista I. (1967). The contribution of altered synapses in the senile plaque: an electron microscopic study in Alzheimer's dementia. J Neuropathol Exp Neurol 26: 25-39 https://doi.org/10.1097/00005072-196701000-00003
  12. Huang YZ, Won S, Ali DW, et al. (2000). Regulation of neuregulin signaling by PSD-95 interacting with ErbB4 at CNS synapses. Neuron 26: 443-455 https://doi.org/10.1016/S0896-6273(00)81176-9
  13. Law AJ, Shannon Weickert C, Hyde TM, Kleinman JE, Harrison PJ. (2004). Neuregulin-1 (NRG-1) mRNA and protein in the adult human brain. Neuroscience 127: 125-136 https://doi.org/10.1016/j.neuroscience.2004.04.026
  14. Lee HJ, Jung KM, Huang YZ, et al. (2002). Presenilin-dependent gamma-secretase-like intramembrane cleavage of ErbB4. J Biol Chem 277: 6318-6323 https://doi.org/10.1074/jbc.M110371200
  15. Li B, Woo RS, Mei L, Malinow R. (2007a). The neuregulin-1 receptor erbB4 controls glutamatergic synapse maturation and plasticity. Neuron 54: 583-597 https://doi.org/10.1016/j.neuron.2007.03.028
  16. Li BS, Ma W, Jaffe H, et al. (2003). Cyclin-dependent kinase-5 is involved in neuregulin-dependent activation of phosphatidylinositol 3-kinase and Akt activity mediating neuronal survival. J Biol Chem 278: 35702-35709 https://doi.org/10.1074/jbc.M302004200
  17. Li Y, Xu Z, Ford GD, et al. (2007b). Neuroprotection by neuregulin-1 in a rat model of permanent focal cerebral ischemia. Brain Res 1184: 277-283 https://doi.org/10.1016/j.brainres.2007.09.037
  18. Lukiw WJ, Bazan NG. (2006). Survival signalling in Alzheimer's disease. Biochem Soc Trans 34: 1277-1282 https://doi.org/10.1042/BST0341277
  19. Marchionni MA, Goodearl AD, Chen MS, et al. (1993). Glial growth factors are alternatively spliced erbB2 ligands expressed in the nervous system. Nature 362: 312-318 https://doi.org/10.1038/362312a0
  20. Mattson MP. (2004). Pathways towards and away from Alzheimer's disease. Nature 430: 631-639 https://doi.org/10.1038/nature02621
  21. Mattson MP, Meffert MK. (2006). Roles for NF-kappaB in nerve cell survival, plasticity, and disease. Cell Death Differ 13: 852-860 https://doi.org/10.1038/sj.cdd.4401837
  22. Meyer D, Birchmeier C. (1995). Multiple essential functions of neuregulin in development. Nature 378: 386-390 https://doi.org/10.1038/378386a0
  23. Murata K, Dalakas MC. (1999). Expression of the costimulatory molecule BB-1, the ligands CTLA-4 and CD28, and their mRNA in inflammatory myopathies. Am J Pathol 155: 453-460 https://doi.org/10.1016/S0002-9440(10)65141-3
  24. Ni CY, Murphy MP, Golde TE, Carpenter G. (2001). gamma -Secretase cleavage and nuclear localization of ErbB-4 receptor tyrosine kinase. Science 294: 2179-2181 https://doi.org/10.1126/science.1065412
  25. Ricart K, J Pearson R Jr, Viera L, et al. (2006). Interactions between beta-neuregulin and neurotrophins in motor neuron apoptosis. J Neurochem 97: 222-233 https://doi.org/10.1111/j.1471-4159.2006.03739.x
  26. Sathasivam S, Ince PG, Shaw PJ. (2001). Apoptosis in amyotrophic lateral sclerosis: a review of the evidence. Neuropathol Appl Neurobiol 27: 257-274 https://doi.org/10.1046/j.0305-1846.2001.00332.x
  27. Shyu WC, Lin SZ, Chiang MF, Yang HI, Thajeb P, Li H. (2004). Neuregulin-1 reduces ischemia-induced brain damage in rats. Neurobiol Aging 25: 935-944 https://doi.org/10.1016/j.neurobiolaging.2003.10.012
  28. Stankovic K, Rio C, Xia A, et al. (2004). Survival of adult spiral ganglion neurons requires erbB receptor signaling in the inner ear. J Neurosci 24: 8651-8661 https://doi.org/10.1523/JNEUROSCI.0733-04.2004
  29. Terry RD, Masliah E, Salmon DP, et al. (1991). Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 30: 572-580 https://doi.org/10.1002/ana.410300410
  30. Woo RS, Li XM, Tao Y, et al. (2007). Neuregulin-1 enhances depolarization-induced GABA release. Neuron 54: 599-610 https://doi.org/10.1016/j.neuron.2007.04.009
  31. Zhang L, Fletcher-Turner A, Marchionni MA, et al. (2004). Neurotrophic and neuroprotective effects of the neuregulin glial growth factor-2 on dopaminergic neurons in rat primary midbrain cultures. J Neurochem 91: 1358-1368 https://doi.org/10.1111/j.1471-4159.2004.02817.x

Cited by

  1. Neuregulin-1 prevents amyloid β-induced impairment of long-term potentiation in hippocampal slices via ErbB4 vol.505, pp.1, 2010, https://doi.org/10.1016/j.neulet.2011.05.246
  2. Neuregulin-1 Exerts Protective Effects Against Neurotoxicities Induced by C-Terminal Fragments of APP via ErbB4 Receptor vol.119, pp.1, 2012, https://doi.org/10.1254/jphs.12057fp
  3. Insights on the functional interactions between miRNAs and copy number variations in the aging brain vol.6, pp.None, 2010, https://doi.org/10.3389/fnmol.2013.00032
  4. Neuregulin1beta1 Antagonizes Apoptosis Via ErbB4-Dependent Activation of PI3-Kinase/Akt in APP/PS1 Transgenic Mice vol.38, pp.11, 2013, https://doi.org/10.1007/s11064-013-1131-z
  5. Fumanjian, a Classic Chinese Herbal Formula, Can Ameliorate the Impairment of Spatial Learning and Memory through Apoptotic Signaling Pathway in the Hippocampus of Rats with Aβ vol.2014, pp.None, 2010, https://doi.org/10.1155/2014/942917
  6. Ameliorative effects and possible molecular mechanisms of action of fibrauretine from Fibraurea recisa Pierre on d-galactose/AlCl3-mediated Alzheimer's disease vol.8, pp.55, 2018, https://doi.org/10.1039/c8ra05356a
  7. Genome-wide association study of Alzheimer's disease endophenotypes at prediagnosis stages vol.14, pp.5, 2010, https://doi.org/10.1016/j.jalz.2017.11.006
  8. Quantification of Tyrosine Hydroxylase and ErbB4 in the Locus Coeruleus of Mood Disorder Patients Using a Multispectral Method to Prevent Interference with Immunocytochemical Signals by Neuromelanin vol.35, pp.2, 2019, https://doi.org/10.1007/s12264-019-00339-y
  9. Centella asiatica Protects D -Galactose/AlCl 3 Mediated Alzheimer’s Disease-Like Rats via PP2A/GSK-3β Signaling Pathway in Their Hippocampus vol.20, pp.8, 2010, https://doi.org/10.3390/ijms20081871
  10. Pathological analysis of ErbB family and NRG-1 protein in progressive supranuclear palsy vol.70, pp.None, 2010, https://doi.org/10.5361/jkmu.70.13
  11. On the Modulatory Roles of Neuregulins/ErbB Signaling on Synaptic Plasticity vol.21, pp.1, 2010, https://doi.org/10.3390/ijms21010275