DOI QR코드

DOI QR Code

Altered expression of parvalbumin immunoreactivity in rat main olfactory bulb following pilocarpine-induced status epilepticus

  • Yu, Yeon Hee (Department of Anatomy, College of Medicine, Soonchunhyang University) ;
  • Park, Dae-Kyoon (Department of Anatomy, College of Medicine, Soonchunhyang University) ;
  • Yoo, Dae Young (Department of Anatomy, College of Medicine, Soonchunhyang University) ;
  • Kim, Duk-Soo (Department of Anatomy, College of Medicine, Soonchunhyang University)
  • Received : 2020.01.03
  • Accepted : 2020.03.12
  • Published : 2020.04.30

Abstract

Epilepsy is a chronic neurological disease characterized by spontaneous recurrent seizures and caused by various factors and mechanisms. Malfunction of the olfactory bulb is frequently observed in patients with epilepsy. However, the morphological changes in the olfactory bulb during epilepsy-induced neuropathology have not been elucidated. Therefore, in the present study, we investigated the expression of parvalbumin (PV), one of the calcium-binding proteins, and morphological changes in the rat main olfactory bulb (MOB) following pilo-carpine-induced status epilepticus (SE). Pilocarpine-induced SE resulted in neuronal degeneration in the external plexiform layer (EPL) and glomerular layer (GL) of the MOB. PV immunoreactivity was observed in the neuronal somas and processes in the EPL and GL of the control group. However, six hours after pilocarpine administration, PV expression was remarkably decreased in the neuronal processes compared to the somas and the average number of PV-positive interneurons was significantly decreased. Three months after pilocarpine treatment, the number of PV-positive interneurons was also significantly decreased compared to the 6 hour group in both layers. In addition, the number of NeuN-positive neurons was also significantly decreased in the EPL and GL following pilocarpine treatment. In double immunofluorescence staining for PV and MAP2, the immunoreactivity for MAP2 around the PV-positive neurons was significantly decreased three months after pilocarpine treatment. Therefore, the present findings suggest that decreases in PV-positive GABAergic interneurons and dendritic density in the MOB induced impaired calcium buffering and reciprocal synaptic transmission. Thus, these alterations may be considered key factors aggravating olfactory function in patients with epilepsy.

Keywords

Acknowledgement

Supported by : National Research Foundation of Korea

References

  1. Al-Mufti F and Claassen J (2014) Neurocritical care: status epilepticus review. Crit Care Clin 30, 751-764 https://doi.org/10.1016/j.ccc.2014.06.006
  2. French JA (2007) Refractory epilepsy: clinical overview. Epilepsia 48, 3-7 https://doi.org/10.1111/j.1528-1167.2007.00992.x
  3. Henshall D (2007) Apoptosis signaling pathways in seizureinduced neuronal death and epilepsy. Biochem Soc Trans 35, 421-423 https://doi.org/10.1042/BST0350421
  4. Wang L, Liu YH, Huang YG and Chen LW (2008) Timecourse of neuronal death in the mouse pilocarpine model of chronic epilepsy using Fluoro-Jade C staining. Brain Res J 1241, 157-167 https://doi.org/10.1016/j.brainres.2008.07.097
  5. Helmstaedter C and Kockelmann E (2006) Cognitive outcomes in patients with chronic temporal lobe epilepsy. Epilepsia 47, 96-98 https://doi.org/10.1111/j.1528-1167.2006.00702.x
  6. Mehla J, Reeta K, Gupta P and Gupta YK (2010) Protective effect of curcumin against seizures and cognitive impairment in a pentylenetetrazole-kindled epileptic rat model. Life Sci 87, 596-603 https://doi.org/10.1016/j.lfs.2010.09.006
  7. Desai M, Agadi J, Karthik N, Praveenkumar S and Netto A (2015) Olfactory abnormalities in temporal lobe epilepsy. J Clin Neurosci 22, 1614-1618 https://doi.org/10.1016/j.jocn.2015.03.035
  8. Imai T (2014) Construction of functional neuronal circuitry in the olfactory bulb. Semin Cell Dev Biol 35, 180-188 https://doi.org/10.1016/j.semcdb.2014.07.012
  9. Hwang IK, Kim DS, Lee HY et al (2003) Age-related Changes of Parvalbumin Immunoreactive Neurons in the Rat Main Olfactory Bulb. Mol Cells 16, 302-306
  10. Caillard O, Moreno H, Schwaller B, Llano I, Celio MR and Marty A (2000) Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity. Proc Natl Acad Sci U S A 97, 13372-13377 https://doi.org/10.1073/pnas.230362997
  11. Choi WS, Chun SY, Markelonis GJ, Oh TH and Oh YJ (2001) Overexpression of calbindin-D28K induces neurite outgrowth in dopaminergic neuronal cells via activation of p38 MAPK. Biochem Biophys Res Commun 287, 656-661 https://doi.org/10.1006/bbrc.2001.5649
  12. Mattson MP (2007) Calcium and neurodegeneration. Aging Cell 6, 337-350 https://doi.org/10.1111/j.1474-9726.2007.00275.x
  13. Kim J, Kwak S, Kim D et al (2006) Reduced calcium binding protein immunoreactivity induced by electroconvulsive shock indicates neuronal hyperactivity, not neuronal death or deactivation. Neuroscience 137, 317-326 https://doi.org/10.1016/j.neuroscience.2005.08.052
  14. Kato HK, Gillet SN, Peters AJ, Isaacson JS and Komiyama T (2013) Parvalbumin-expressing interneurons linearly control olfactory bulb output. Neuron 80, 1218-1231 https://doi.org/10.1016/j.neuron.2013.08.036
  15. Kovac S, Domijan A, Walker M and Abramov A (2014) Seizure activity results in calcium-and mitochondria-independent ROS production via NADPH and xanthine oxidase activation. Cell Death Dis 5, e1442 https://doi.org/10.1038/cddis.2014.390
  16. Gonzalez-Reyes S, Santillan-Cigales JJ, Jimenez-Osorio AS, Pedraza-Chaverri J and Guevara-Guzman R (2016) Glycyrrhizin ameliorates oxidative stress and inflammation in hippocampus and olfactory bulb in lithium/pilocarpine-induced status epilepticus in rats. Epilepsy Res 126, 126-133 https://doi.org/10.1016/j.eplepsyres.2016.07.007
  17. Hummel T, Henkel S, Negoias S et al (2013) Olfactory bulb volume in patients with temporal lobe epilepsy. J Neurol 260, 1004-1008
  18. Nguyen MQ and Ryba NJ (2012) A smell that causes seizure. PLoS One 7, e41899 https://doi.org/10.1371/journal.pone.0041899
  19. Suzuki Y, Kiyokage E, Sohn J, Hioki H and Toida K (2015) Structural basis for serotonergic regulation of neural circuits in the mouse olfactory bulb. J Comp Neurol 523, 262-280 https://doi.org/10.1002/cne.23680
  20. Egger V and Urban NN (2006) Dynamic connectivity in mitral cell-granule cell microcircuit. Semin Cell Dev Biol 17, 424-432 https://doi.org/10.1016/j.semcdb.2006.04.006
  21. Isaacson JS and Strowbridge BW (1998) Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron 20, 749-761 https://doi.org/10.1016/S0896-6273(00)81013-2
  22. Schwaller B, Meyer M and Schiffmann S (2002) 'New' functions for 'old'proteins: the role of the calcium-binding proteins calbindin D-28k, calretinin and parvalbumin, in cerebellar physiology. Studies with knockout mice. Cerebellum 1, 241-258 https://doi.org/10.1080/147342202320883551
  23. Schwaller B (2009) The continuing disappearance of "pure" Ca 2+ buffers. Cell Mol Life Sci 66, 275-300 https://doi.org/10.1007/s00018-008-8564-6
  24. Yu L, Xu L, Xu M, Wan B, Yu L and Huang Q (2011) Role of Mg2+ ions in protein kinase phosphorylation: insights from molecular dynamics simulations of ATP-kinase complexes. Mol Simul 37, 1143-1150 https://doi.org/10.1080/08927022.2011.561430
  25. Konur S and Ghosh A (2005) Calcium signaling and the control of dendritic development. Neuron 46, 401-405 https://doi.org/10.1016/j.neuron.2005.04.022
  26. Yuste R and Bonhoeffer T (2001) Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 24, 1071-1089
  27. Sjostrom PJ, Rancz EA, Roth A and Hausser M (2008) Dendritic excitability and synaptic plasticity. Physiol Rev 88, 769-840 https://doi.org/10.1152/physrev.00016.2007
  28. Kim DS, Kim JE, Kwak SE et al (2008) Spatiotemporal characteristics of astroglial death in the rat hippocampoentorhinal complex following pilocarpine-induced status epilepticus. J Comp Neurol 511, 581-598 https://doi.org/10.1002/cne.21851
  29. Schmued LC and Hopkinsa CJ (2000) Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res J 874, 123-130 https://doi.org/10.1016/S0006-8993(00)02513-0
  30. Jung HY, Kim DW, Nam SM et al (2017) Pyridoxine improves hippocampal cognitive function via increases of serotonin turnover and tyrosine hydroxylase, and its association with CB1 cannabinoid receptor-interacting protein and the CB1 cannabinoid receptor pathway. Biochim Biophys Acta Gen Subj 1861, 3142-3153 https://doi.org/10.1016/j.bbagen.2017.09.006