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Changes in the Neurogenesis and Axonal Sprouting in the Organotypic Hippocampal Slice Culture by Aβ25-35 Treatment

  • Jung, Yeon Joo (Department of Pharmacology and Ewha Medical Research Institute, Ewha Womans University School of Medicine) ;
  • Jiang, Hui Ling (Department of Pharmacology and Ewha Medical Research Institute, Ewha Womans University School of Medicine) ;
  • Lee, Kyung Eun (Department of Pharmacology and Ewha Medical Research Institute, Ewha Womans University School of Medicine)
  • Received : 2012.11.09
  • Accepted : 2012.12.05
  • Published : 2012.12.31

Abstract

Induction of neurogenesis can occur in the hippocampus in response to various pathological conditions, such as Alzheimer's disease. The aim of this study was to investigate the changes that occur in endogenous neural stem cells in response to amyloid beta $(A{\beta})_{25-35}$-induced neuronal cell damage in organotypic hippocampal slice cultures. Cresyl violet staining and Fluoro-Jade B staining were used to detect neuronal cell damage and changes of mossy fiber terminals were observed by Timm's staining. The immunofl uorescence staining was used to detect the newly generated cells in the subgranular zone (SGZ) of the dentate gyrus with specific marker, 5-bromo-2'-deoxyuridine (BrdU), Ki-67, Nestin, and doublecortin (DCX). In compared to control slices, neuronal cell damage was observed and the mossy fibers were expanded to CA3 area by treatment with $A{\beta}_{25-35}$. Ki-67/Nestin- and BrdU/DCX-positive cells were detected in the SGZ. In conclusion, these results demonstrate that $A{\beta}$-induced neuronal damage results in an increase in endogenous neural stem cells in rat hippocampal slice cultures not only for gliosis but also for neurogenesis.

Keywords

References

  1. Bjorklund N L, Reese L C, Sadagoparamanujam V M, Ghirardi V, Woltjer R L, and Taglialatela G (2012) Absence of amyloid beta oligomers at the postsynapse and regulated synaptic Zn2+ in cognitively intact aged individuals with Alzheimer's disease neuropathology. Mol. Neurodegener 7, 23. https://doi.org/10.1186/1750-1326-7-23
  2. Bunk E C, Konig H G, Bonner H P, Kirby B P, and Prehn J H (2010) NMDA-induced injury of mouse organotypic hippocampal slice cultures triggers delayed neuroblast proliferation in the dentate gyrus: an in vitro model for the study of neural precursor cell proliferation. Brain Res. 1359, 22-32. https://doi.org/10.1016/j.brainres.2010.05.024
  3. Bush A I, Pettingell W H, Multhaup G, d Paradis M, Vonsattel J P, Gusella J F, Beyreuther K, Masters C L, and Tanzi R E (1994) Rapid induction of Alzheimer A beta amyloid formation by zinc. Science 265, 1464- 1467. https://doi.org/10.1126/science.8073293
  4. Chechneva O, Dinkel K, Schrader D, and Reymann K G (2005) Identification and characterization of two neurogenic zones in interface organotypic hippocampal slice cultures. Neuroscience 136, 343-355. https://doi.org/10.1016/j.neuroscience.2005.07.058
  5. Chuang T T (2010) Neurogenesis in mouse models of Alzheimer's disease. BBA 1802, 872-880. https://doi.org/10.1016/j.bbadis.2009.12.008
  6. Dehghani F, Hischebeth G T, Wirjatijasa F, Kohl A, Korf H W, and Hailer N P (2003) The immunosuppressant mycophenolate mofetil attenuates neuronal damage after excitotoxic injury in hippocampal slice cultures. Eur. J. Neurosci. 18, 1061-1072. https://doi.org/10.1046/j.1460-9568.2003.02821.x
  7. Deshpande A, Kawai H, Metherate R, Glabe C G, and Busciglio J (2009) A role for synaptic zinc in activity-dependent Abeta oligomer formation and accumulation at excitatory synapses. J. neurosci. 29, 4004- 4015. https://doi.org/10.1523/JNEUROSCI.5980-08.2009
  8. Eriksson P S, Perfilieva E, Bjork-Eriksson T, Alborn A M, Nordborg C, Peterson D A, and Gage F H (1998) Neurogenesis in the adult human hippocampus. Nat. Med. 4, 1313-1317. https://doi.org/10.1038/3305
  9. Faller P (2009) Copper and zinc binding to amyloid-beta: coordination, dynamics, aggregation, reactivity and metal-ion transfer. Chembiochem: Eur. J. Chem. Biol. 10, 2837-2845. https://doi.org/10.1002/cbic.200900321
  10. Haughey N J, Liu D, Nath A, Borchard A C, and Mattson M P (2002) Disruption of neurogenesis in the subventricular zone of adult mice, and in human cortical neuronal precursor cells in culture, by amyloid beta-peptide: implications for the pathogenesis of Alzheimer's disease. Neuromolecular Med. 1, 125-135. https://doi.org/10.1385/NMM:1:2:125
  11. Haydar T F, Bambrick L L, Krueger B K, and Rakic P (1999) Organotypic slice cultures for analysis of proliferation, cell death, and migration in the embryonic neocortex. Brain Res. 4, 425-437.
  12. Heo C, Chang K A, Choi H S, Kim H S, Kim S, Liew H, Kim J A, Yu E, Ma J, and Suh Y H (2007) Effects of the monomeric, oligomeric, and fi brillar Abeta42 peptides on the proliferation and differentiation of adult neural stem cells from subventricular zone. J. Neurochem. 102, 493-500. https://doi.org/10.1111/j.1471-4159.2007.04499.x
  13. Huang E P (1997) Metal ions and synaptic transmission: think zinc. Proc. Natl. Acad. Sci. U S A 94, 13386-13387. https://doi.org/10.1073/pnas.94.25.13386
  14. Kuan C Y, Schloemer A J, Lu A, Burns K A, Weng W L, Williams M T, Strauss K I, Vorhees C V, Flavell R A, Davis R J, Sharp F R, and Rakic P (2004) Hypoxia-ischemia induces DNA synthesis without cell proliferation in dying neurons in adult rodent brain. J. Neurosci. 24, 10763-10772. https://doi.org/10.1523/JNEUROSCI.3883-04.2004
  15. Lie D C, Song H, Colamarino S A, Ming G L, and Gage F H (2004) Neurogenesis in the adult brain: new strategies for central nervous system diseases. Ann. Rev. Pharm. Toxicol. 44, 399-421. https://doi.org/10.1146/annurev.pharmtox.44.101802.121631
  16. Lopez-Toledano M A and Shelanski M L (2004) Neurogenic effect of betaamyloid peptide in the development of neural stem cells. J. Neurosci. 24, 5439-5444. https://doi.org/10.1523/JNEUROSCI.0974-04.2004
  17. Lopez-Toledano M A and Shelanski M L (2007) Increased neurogenesis in young transgenic mice overexpressing human APP(Sw, Ind). J. Alzheimer's Dis. 12, 229-240. https://doi.org/10.3233/JAD-2007-12304
  18. Mattson M P (2000) Apoptosis in neurodegenerative disorders. Nat. Rev. Mol. Cell Bio. 1, 120-129. https://doi.org/10.1038/35040009
  19. Mazur-Kolecka B, Golabek A, Nowicki K, Flory M, and Frackowiak J (2006) Amyloid-beta impairs development of neuronal progenitor cells by oxidative mechanisms. Neurobiol. Aging 27, 1181-1192. https://doi.org/10.1016/j.neurobiolaging.2005.07.006
  20. Namba T, Mochizuki H, Onodera M, Namiki H, and Seki T (2007) Postnatal neurogenesis in hippocampal slice cultures: early in vitro labeling of neural precursor cells leads to efficient neuronal production. J. Neurosci. Res. 85, 1704-1712. https://doi.org/10.1002/jnr.21295
  21. Perez-Gomez A and Tasker R A (2012) Enhanced neurogenesis in organotypic cultures of rat hippocampus after transient subfieldselective excitotoxic insult induced by domoic acid. Neuroscience 208, 97-108. https://doi.org/10.1016/j.neuroscience.2012.02.003
  22. Picard-Riera N, Nait-Oumesmar B, and Baron-Van Evercooren A (2004) Endogenous adult neural stem cells: limits and potential to repair the injured central nervous system. J. Neurosci. Res. 76, 223-231. https://doi.org/10.1002/jnr.20040
  23. Plumpe T, Ehninger D, Steiner B, Klempin F, Jessberger S, Brandt M, Romer B, Rodriguez G R, Kronenberg G, and Kempermann G (2006) Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci. 7, 77. https://doi.org/10.1186/1471-2202-7-77
  24. Raineteau O, Rietschin L, Gradwohl G, Guillemot F, and Gahwiler BH (2004) Neurogenesis in hippocampal slice cultures. Mol. Cell. Neurosci. 26, 241-250. https://doi.org/10.1016/j.mcn.2004.01.003
  25. Religa D, Strozyk D, Cherny R A, Volitakis I, Haroutunian V, Winblad B, Naslund J, and Bush A I (2006) Elevated cortical zinc in Alzheimer disease. Neurology 67, 69-75. https://doi.org/10.1212/01.wnl.0000223644.08653.b5
  26. Rodriguez J J, Jones V C, and Verkhratsky A (2009) Impaired cell proliferation in the subventricular zone in an Alzheimer's disease model. Neuroreport 20, 907-912. https://doi.org/10.1097/WNR.0b013e32832be77d
  27. Rola R, Raber J, Rizk A, Otsuka S, VandenBerg S R, Morhardt D R, and Fike J R (2004) Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive defi cits in young mice. Exp. Neurol. 188, 316-330. https://doi.org/10.1016/j.expneurol.2004.05.005
  28. Sadgrove M P, Laskowski A, and Gray W P (2006) Examination of granule layer cell count, cell density, and single-pulse BrdU incorporation in rat organotypic hippocampal slice cultures with respect to culture medium, septotemporal position, and time in vitro. J. Comp. Neurol. 497, 397-415. https://doi.org/10.1002/cne.21000
  29. Scheffl er B, Schmandt T, Schroder W, Steinfarz B, Husseini L, Wellmer J, Seifert G, Karram K, Beck H, Blumcke I, Wiestler O D, Steinhauser C, and Brustle O (2003) Functional network integration of embryonic stem cell-derived astrocytes in hippocampal slice cultures. Development (Cambridge, England) 130, 5533-5541. https://doi.org/10.1242/dev.00714
  30. Schaffer D V and Gage F H (2004) Neurogenesis and neuroadaptation. Neuromolecular Med. 5, 1-9. https://doi.org/10.1385/NMM:5:1:001
  31. Suh E C, Jung Y J, Kim Y A, Park E M, and Lee K E (2008) A beta 25- 35 induces presynaptic changes in organotypic hippocampal slice cultures. Neurotoxicology 29, 691-699. https://doi.org/10.1016/j.neuro.2008.04.001
  32. Tamura M, Koyama R, Ikegaya Y, Matsuki N, and Yamada M K (2006) K252a, an inhibitor of Trk, disturbs pathfinding of hippocampal mossy fibers. Neuroreport 17, 481-486. https://doi.org/10.1097/01.wnr.0000208997.23448.ea
  33. Tanaka A, Watanabe Y, Kato H, and Araki T (2007) Immunohistochemical changes related to ageing in the mouse hippocampus and subventricular zone. Mech. Ageing Dev. 128, 303-310. https://doi.org/10.1016/j.mad.2007.01.002
  34. Tanvig M, Blaabjerg M, Andersen R K, Villa A, Rosager A M, Poulsen F R, Martinez-Serrano A, Zimmer J, and Meyer M (2009) A brain slice culture model for studies of endogenous and exogenous precursor cell migration in the rostral migratory stream. Brain Res. 1295, 1-12. https://doi.org/10.1016/j.brainres.2009.07.075
  35. Wang J M, Irwin R W, Liu L, Chen S, and Brinton R D (2007) Regeneration in a degenerating brain: potential of allopregnanolone as a neuroregenerative agent. Curr. Alzheimer Res. 4, 510-517. https://doi.org/10.2174/156720507783018262
  36. Wang S H, Zhang Z J, Guo Y J, Teng G J, and Chen B A (2008) Hippocampal neurogenesis and behavioural studies on adult ischemic rat response to chronic mild stress. Behav. Brain Res. 189, 9-16. https://doi.org/10.1016/j.bbr.2007.11.028
  37. Zhang C, McNeil E, Dressler L, and Siman R (2007) Long-lasting impairment in hippocampal neurogenesis associated with amyloid deposition in a knock-in mouse model of familial Alzheimer's disease. Exp. Neurol. 204, 77-87. https://doi.org/10.1016/j.expneurol.2006.09.018
  38. Ziabreva I, Perry E, Perry R, Minger S L, Ekonomou A, Przyborski S, and Ballard C (2006) Altered neurogenesis in Alzheimer's disease. J. Psychosom. Res. 61, 311-316. https://doi.org/10.1016/j.jpsychores.2006.07.017