Chronic ketamine produces altered distribution of parvalbumin-positive cells in the hippocampus of adult rats

Neuroscience Letters

Volumn 550, Issue , 2013, Pages 69-74

  Sabbagh, Jonathan J ^a   Murtishaw, Andrew S ^a   Bolton, Monica M ^a   Heaney, Chelcie F ^a   Langhardt, Michael ^a   Kinney, Jefferson W ^a  

^a UNIVERSITY OF NEVADA   (United States)

Author keywords

Hippocampus; Ketamine; Parvalbumin; Schizophrenia

Indexed keywords

KETAMINE; PARVALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL COUNT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HIPPOCAMPAL CA3 REGION; IMMUNOHISTOCHEMISTRY; INTERNEURON; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RETROSPLENIAL CORTEX; SCHIZOPHRENIA; SENSORY GATING; SPATIAL LEARNING; STRATUM ORIENS;

HIPPOCAMPUS; KETAMINE; PARVALBUMIN; SCHIZOPHRENIA;

ANIMALS; CELL MOVEMENT; DISEASE MODELS, ANIMAL; EXCITATORY AMINO ACID ANTAGONISTS; HIPPOCAMPUS; KETAMINE; MALE; MAZE LEARNING; NEURONS; PARVALBUMINS; RATS; RATS, SPRAGUE-DAWLEY; SCHIZOPHRENIA;

EID: 84881371438     PISSN: 03043940     EISSN: 18727972     Source Type: Journal    
DOI: 10.1016/j.neulet.2013.06.040     Document Type: Article

References (50)

1. Akbarian S., Sucher N.J., Bradley D., Tafazzoli A., Trinh D., Hetrick W.P., Potkin S.G., Sandman C.A., Bunney W.E., Jones E.G. Selective alterations in gene expression for NMDA receptor subunits in prefrontal cortex of schizophrenics. J. Neurosci. 1996, 16(1):19-30.
2. Beasley C.L., Reynolds G.P. Parvalbumin-immunoreactive neurons are reduced in the prefrontal cortex of schizophrenics. Schizophr. Res. 1997, 24(3):349-355.
3. Becker A., Peters B., Schroeder H., Mann T., Huether G., Grecksch G. Ketamine-induced changes in rat behaviour: a possible animal model of schizophrenia. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 2003, 27(4):687-700.
4. Beneyto M., Kristiansen L.V., Oni-Orisan A., McCullumsmith R.E., Meador-Woodruff J.H. Abnormal glutamate receptor expression in the medial temporal lobe in schizophrenia and mood disorders. Neuropsychopharmacology 2007, 32(9):1888-1902.
5. Bolton M.M., Heaney C.F., Sabbagh J.J., Murtishaw A.S., Magcalas C.M., Kinney J.W. Deficits in emotional learning and memory in an animal model of schizophrenia. Behav. Brain Res. 2012, 233(1):35-44.
6. Bullock W.M., Cardon K., Bustillo J., Roberts R.C., Perrone-Bizzozero N.I. Altered expression of genes involved in GABAergic transmission and neuromodulation of granule cell activity in the cerebellum of schizophrenia patients. Am. J. Psychiatry 2008, 165(12):1594-1603.
7. Callicott J.H., Straub R.E., Pezawas L., Egan M.F., Mattay V.S., Hariri A.R., Verchinski B.A., Meyer-Lindenberg A., Balkissoon R., Kolachana B., Goldberg T.E., Weinberger D.R. Variation in DISC1 affects hippocampal structure and function and increases risk for schizophrenia. Proc. Natl. Acad. Sci. U.S.A. 2005, 102(24):8627-8632.
8. Cilia J., Hatcher P., Reavill C., Jones D.N.C. (±) Ketamine-induced prepulse inhibition deficits of an acoustic startle response in rats are not reversed by antipsychotics. J. Psychopharmacol. 2007, 21(3):302-311.
9. D'Arcangelo G., Miao G.G., Chen S.C., Soares H.D., Morgan J.I., Curran T. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 1995, 374(6524):719-723.
10. Duan X., Chang J.H., Ge S., Faulkner R.L., Kim J.Y., Kitabatake Y., Liu X.B., Yang C.H., Jordan J.D., Ma D.K., Liu C.Y., Ganesan S., Cheng H.J., Ming G.L., Lu B., Song H. Disrupted-in-schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell 2007, 130(6):1146-1158.
11. Eastwood S.L., Harrison P.J. Decreased expression of vesicular glutamate transporter 1 and complexin II mRNAs in schizophrenia: further evidence for a synaptic pathology affecting glutamate neurons. Schizophr. Res. 2005, 73(2-3):159-172.
12. Fatemi S.H., Earle J.A., McMenomy T. Reduction in Reelin immunoreactivity in hippocampus of subjects with schizophrenia, bipolar disorder and major depression. Mol. Psychiatry 2000, 5(6):654-663. 571.
13. Gao X., Sakai K., Roberts R.C., Conley R.R., Dean B., Tamminga C.A. Ionotropic glutamate receptors and expression of N-methyl-d-aspartate receptor subunits in subregions of human hippocampus: effects of schizophrenia. Am. J. Psychiatry 2000, 157(7):1141-1149.
14. Guidotti A., Auta J., Davis J.M., Di-Giorgi-Gerevini V., Dwivedi Y., Grayson D.R., Impagnatiello F., Pandey G., Pesold C., Sharma R., Uzunov D., Costa E. Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder: a postmortem brain study. Arch. Gen. Psychiatry 2000, 57(11):1061-1069.
15. Hashimoto T., Volk D.W., Eggan S.M., Mirnics K., Pierri J.N., Sun Z., Sampson A.R., Lewis D.A. Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J. Neurosci. 2003, 23(15):6315-6326.
16. Hiesberger T., Trommsdorff M., Howell B.W., Goffinet A., Mumby M.C., Cooper J.A., Herz J. Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 1999, 24(2):481-489.
17. Impagnatiello F., Guidotti A.R., Pesold C., Dwivedi Y., Caruncho H., Pisu M.G., Uzunov D.P., Smalheiser N.R., Davis J.M., Pandey G.N., Pappas G.D., Tueting P., Sharma R.P., Costa E. A decrease of reelin expression as a putative vulnerability factor in schizophrenia. Proc. Natl. Acad. Sci. U.S.A. 1998, 95(26):15718-15723.
18. Jakob H., Beckmann H. Circumscribed malformation and nerve cell alterations in the entorhinal cortex of schizophrenics. Pathogenetic and clinical aspects. J. Neural Transm. Gen. Sect. 1994, 98(2):83-106.
19. Jentsch J.D., Roth R.H. The neuropsychopharmacology of phencyclidine: from NMDA receptor hypofunction to the dopamine hypothesis of schizophrenia. Neuropsychopharmacology 1999, 20(3):201-225.
20. Kahler A.K., Djurovic S., Kulle B., Jonsson E.G., Agartz I., Hall H., Opjordsmoen S., Jakobsen K.D., Hansen T., Melle I., Werge T., Steen V.M., Andreassen O.A. Association analysis of schizophrenia on 18 genes involved in neuronal migration: MDGA1 as a new susceptibility gene. Am. J. Med. Genet. B: Neuropsychiatr. Genet. 2008, 147B(7):1089-1100.
21. Kang W.Y., Kim S.S., Cho S.K., Kim S., Suh-Kim H., Lee Y.D. Migratory defect of mesencephalic dopaminergic neurons in developing reeler mice. Anat. Cell Biol. 2010, 43(3):241-251.
22. Keilhoff G., Becker A., Grecksch G., Wolf G., Bernstein H.G. Repeated application of ketamine to rats induces changes in the hippocampal expression of parvalbumin, neuronal nitric oxide synthase and cFOS similar to those found in human schizophrenia. Neuroscience 2004, 126(3):591-598.
23. Keilhoff G., Bernstein H.G., Becker A., Grecksch G., Wolf G. Increased neurogenesis in a rat ketamine model of schizophrenia. Biol. Psychiatry 2004, 56(5):317-322.
24. Kim J.Y., Duan X., Liu C.Y., Jang M.H., Guo J.U., Pow-anpongkul N., Kang E., Song H., Ming G.L. DISC1 regulates new neuron development in the adult brain via modulation of AKT-mTOR signaling through KIAA1212. Neuron 2009, 63(6):761-773.
25. Kinney J.W., Davis C.N., Tabarean I., Conti B., Bartfai T., Behrens M.M. A specific role for NR2A-containing NMDA receptors in the maintenance of parvalbumin and GAD67 immunoreactivity in cultured interneurons. J. Neurosci. 2006, 26(5):1604-1615.
26. Konradi C., Yang C.K., Zimmerman E.I., Lohmann K.M., Gresch P., Pantazopoulos H., Berretta S., Heckers S. Hippocampal interneurons are abnormal in schizophrenia. Schizophr. Res. 2011, 131(1-3):165-173.
27. Kvajo M., McKellar H., Arguello P.A., Drew L.J., Moore H., MacDermott A.B., Karayiorgou M., Gogos J.A. A mutation in mouse Disc1 that models a schizophrenia risk allele leads to specific alterations in neuronal architecture and cognition. Proc. Natl. Acad. Sci. U.S.A. 2008, 105(19):7076-7081.
28. Lahti A.C., Weiler M.A., Michaelidis T., Parwani A., Tamminga C.A. Effects of ketamine in normal and schizophrenic volunteers. Neuropsychopharmacology 2001, 25(4):455-467.
29. Lewis D.A., Hashimoto T., Volk D.W. Cortical inhibitory neurons and schizophrenia. Nat. Rev. Neurosci. 2005, 6(4):312-324.
30. Li J., Liu J., Feng G., Li T., Zhao Q., Li Y., Hu Z., Zheng L., Zeng Z., He L., Wang T., Shi Y. The MDGA1 gene confers risk to schizophrenia and bipolar disorder. Schizophr. Res. 2011, 125(2-3):194-200.
31. Manning E.E., Ransome M.I., Burrows E.L., Hannan A.J. Increased adult hippocampal neurogenesis and abnormal migration of adult-born granule neurons is associated with hippocampal-specific cognitive deficits in phospholipase C-beta1 knockout mice. Hippocampus 2012, 22(2):309-319.
32. McBain C.J., Fisahn A. Interneurons unbound. Nat. Rev. Neurosci. 2001, 2(1):11-23.
33. Meechan D.W., Tucker E.S., Maynard T.M., LaMantia A.S. Diminished dosage of 22q11 genes disrupts neurogenesis and cortical development in a mouse model of 22q11 deletion/DiGeorge syndrome. Proc. Natl. Acad. Sci. U.S.A. 2009, 106(38):16434-16445.
34. Mercer A., Eastlake K., Trigg H.L., Thomson A.M. Local circuitry involving parvalbumin-positive basket cells in the CA2 region of the hippocampus. Hippocampus 2012, 22(1):43-56.
35. Moller H.- The psychopathology of schizophrenia: An integrated view on positive symptoms and negative symptoms. Int. Clin. Psychopharmacol. 1995, 10(Suppl. 3):57-64.
36. Namba T., Ming G.L., Song H., Waga C., Enomoto A., Kaibuchi K., Kohsaka S., Uchino S. NMDA receptor regulates migration of newly generated neurons in the adult hippocampus via disrupted-in-schizophrenia 1 (DISC1). J. Neurochem. 2011, 118(1):34-44.
37. Neill J.C., Barnes S., Cook S., Grayson B., Idris N.F., McLean S.L., Snigdha S., Rajagopal L., Harte M.K. Animal models of cognitive dysfunction and negative symptoms of schizophrenia: focus on NMDA receptor antagonism. Pharmacol. Ther. 2010, 128(3):419-432.
38. Nullmeier S., Panther P., Dobrowolny H., Frotscher M., Zhao S., Schwegler H., Wolf R. Region-specific alteration of GABAergic markers in the brain of heterozygous reeler mice. Eur. J. Neurosci. 2011, 33(4):689-698.
39. Pesold C., Impagnatiello F., Pisu M.G., Uzunov D.P., Costa E., Guidotti A., Caruncho H.J. Reelin is preferentially expressed in neurons synthesizing gamma-aminobutyric acid in cortex and hippocampus of adult rats. Proc. Natl. Acad. Sci. U.S.A. 1998, 95(6):3221-3226.
40. Powell S.B., Sejnowski T.J., Behrens M.M. Behavioral and neurochemical consequences of cortical oxidative stress on parvalbumin-interneuron maturation in rodent models of schizophrenia. Neuropharmacology 2012, 62(3):1322-1331.
41. Reiprich P., Kilb W., Luhmann H.J. Neonatal NMDA receptor blockade disturbs neuronal migration in rat somatosensory cortex in vivo. Cereb. Cortex 2005, 15(3):349-358.
42. Sabbagh J.J., Heaney C.F., Bolton M.M., Murtishaw A.S., Kinney J.W. Examination of ketamine-induced deficits in sensorimotor gating and spatial learning. Physiol. Behav. 2012, 107(3):355-363.
43. Sloviter R.S. Calcium-binding protein (calbindin-D28k) and parvalbumin immunocytochemistry: localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. J. Comp. Neurol. 1989, 280(2):183-196.
44. Swerdlow N.R., Bakshi V., Waikar M., Taaid N., Geyer M.A. Seroquel, clozapine and chlorpromazine restore sensorimotor gating in ketamine-treated rats. Psychopharmacology (Berl) 1998, 140(1):75-80.
45. Tomita K., Kubo K., Ishii K., Nakajima K. Disrupted-in-schizophrenia-1 (Disc1) is necessary for migration of the pyramidal neurons during mouse hippocampal development. Hum. Mol. Genet. 2011, 20(14):2834-2845.
46. Uhlhaas P.J., Haenschel C., Nikolic D., Singer W. The role of oscillations and synchrony in cortical networks and their putative relevance for the pathophysiology of schizophrenia. Schizophr. Bull. 2008, 34(5):927-943.
47. van Berckel B.N., Oranje B., van Ree J.M., Verbaten M.N., Kahn R.S. The effects of low dose ketamine on sensory gating, neuroendocrine secretion and behavior in healthy human subjects. Psychopharmacology (Berl) 1998, 137(3):271-281.
48. Volman V., Behrens M.M., Sejnowski T.J. Downregulation of parvalbumin at cortical GABA synapses reduces network gamma oscillatory activity. J. Neurosci. 2011, 31(49):18137-18148.
49. Woo T.-W., Kim A.M., Viscidi E. Disease-specific alterations in glutamatergic neurotransmission on inhibitory interneurons in the prefrontal cortex in schizophrenia. Brain Res. 2008, 1218 (C):267-277.
50. Zhang Z.J., Reynolds G.P. A selective decrease in the relative density of parvalbumin-immunoreactive neurons in the hippocampus in schizophrenia. Schizophr. Res. 2002, 55(1-2):1-10.