Electroconvulsive Seizures Stimulate Glial Proliferation and Reduce Expression of Sprouty2 within the Prefrontal Cortex of Rats

Biological Psychiatry

Volumn 62, Issue 5, 2007, Pages 505-512

  Öngür, Dost ^a   Pohlman, Jessica ^a   Dow, Antonia L ^a   Eisch, Amelia J ^b   Edwin, Francis ^c   Heckers, Stephan ^a   Cohen, Bruce M ^a   Patel, Tarun B ^c   Carlezon Jr , William A ^a  

^a MCLEAN HOSPITAL   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c LOYOLA UNIVERSITY CHICAGO   (United States)

Author keywords

Bipolar disorder; depression; electroconvulsive seizure; glia; infralimbic prefrontal cortex; NG2; Sprouty

Indexed keywords

BROXURIDINE; CELL MARKER; CYCLINE; SPROUTY 2 PROTEIN; SPROUTY PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN NERVE CELL; CELL COUNT; CELL LABELING; CELL PROLIFERATION; CONTROLLED STUDY; CONVULSION; DENSITY; ENDOTHELIUM CELL; GLIA CELL; IMMUNOCOMPETENT CELL; LIMBIC CORTEX; MALE; NONHUMAN; OLIGODENDROGLIA; PHENOTYPE; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPRAGUE DAWLEY RAT; SURVIVAL TIME;

ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS; BROMODEOXYURIDINE; CELL COUNT; CELL PROLIFERATION; ELECTROSHOCK; GENE EXPRESSION REGULATION; MALE; NERVE TISSUE PROTEINS; NEUROGLIA; NEURONS; PREFRONTAL CORTEX; PROTEOGLYCANS; RATS; RATS, SPRAGUE-DAWLEY; SEIZURES;

EID: 34548009165     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2006.11.014     Document Type: Article

References (57)

1. Altar C.A., Laeng P., Jurata L.W., Brockman J.A., Lemire A., Bullard J., et al. Electroconvulsive seizures regulate gene expression of distinct neurotrophic signaling pathways. J Neurosci 24 (2004) 2667-2677
2. Belachew S., Chittajallu R., Aguirre A.A., Yuan X., Kirby M., Anderson S., et al. Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. J Cell Biol 161 (2003) 169-186
3. Bergles D.E., Roberts J.D., Somogyi P., and Jahr C.E. Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405 (2000) 187-191
4. Cabrita M.A., and Christofori G. Sprouty proteins: antagonists of endothelial cell signaling and more. Thromb Haemost 90 (2003) 586-590
5. Carlezon Jr. W.A., Boundy V.A., Haile C.N., Lane S.B., Kalb R.G., Neve R.L., et al. Sensitization to morphine induced by viral-mediated gene transfer. Science 277 (1997) 812-814
6. Chambers D., and Mason I. Expression of sprouty2 during early development of the chick embryo is coincident with known sites of FGF signalling. Mech Dev 91 (2000) 361-364
7. Coyle J.T., and Duman R.S. Finding the intracellular signaling pathways affected by mood disorder treatments. Neuron 38 (2003) 157-160
8. Dayer A.G., Cleaver K.M., Abouantoun T., and Cameron H.A. New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors. J Cell Biol 168 (2005) 415-427
9. Drevets W.C. Neuroimaging studies of mood disorders. Biol Psychiatry 48 (2000) 813-829
10. Drevets W.C., Price J.L., Simpson J.R., Todd R.D., Reich T., Vannier M., et al. Subgenual prefrontal cortex abnormalities in mood disorders. Nature 386 (1997) 824-827
11. Drevets W.C., Videen T.O., Price J.L., Preskorn S.H., Carmichael S.T., and Raichle M.E. A functional anatomical study of unipolar depression. J Neurosci 12 (1992) 3628-3641
12. Duman R.S. Depression: a case of neuronal life and death?. Biol Psychiatry 56 (2004) 140-145
13. Edwin F., Singh R., Endersby R., Baker S.J., and Patel T.B. The tumor suppressor PTEN is necessary for human Sprouty 2-mediated inhibition of cell proliferation. J Biol Chem 281 (2006) 4816-4822
14. Gage F.H. Neurogenesis in the adult brain. J Neurosci 22 (2002) 612-613
15. Gross I., Bassit B., Benezra M., and Licht J.D. Mammalian sprouty proteins inhibit cell growth and differentiation by preventing ras activation. J Biol Chem 276 (2001) 46460-46468
16. Gundersen H.J., Bagger P., Bendtsen T.F., Evans S.M., Korbo L., Marcussen N., et al. The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. Apmis 96 (1988) 857-881
17. Hacohen N., Kramer S., Sutherland D., Hiromi Y., and Krasnow M.A. sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 92 (1998) 253-263
18. Hellsten J., Wennstrom M., Mohapel P., Ekdahl C.T., Bengzon J., and Tingstrom A. Electroconvulsive seizures increase hippocampal neurogenesis after chronic corticosterone treatment. Eur J Neurosci 16 (2002) 283-290
19. Horner P.J., Thallmair M., and Gage F.H. Defining the NG2-expressing cell of the adult CNS. J Neurocytol 31 (2002) 469-480
20. Impagnatiello M.A., Weitzer S., Gannon G., Compagni A., Cotten M., and Christofori G. Mammalian sprouty-1 and -2 are membrane-anchored phosphoprotein inhibitors of growth factor signaling in endothelial cells. J Cell Biol 152 (2001) 1087-1098
21. Kim H.J., and Bar-Sagi D. Modulation of signalling by Sprouty: a developing story. Nat Rev Mol Cell Biol 5 (2004) 441-450
22. Kramer S., Okabe M., Hacohen N., Krasnow M.A., and Hiromi Y. Sprouty: a common antagonist of FGF and EGF signaling pathways in Drosophila. Development 126 (1999) 2515-2525
23. Krettek J.E., and Price J.L. The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J Comparative Neurol 171 (1977) 157-191
24. Lane R.D., Reiman E.M., Ahern G.L., Schwartz G.E., and Davidson R.J. Neuroanatomical correlates of happiness, sadness, and disgust. Am J Psychiatry 154 (1997) 926-933
25. Lee S.H., Schloss D.J., Jarvis L., Krasnow M.A., and Swain J.L. Inhibition of angiogenesis by a mouse sprouty protein. J Biol Chem 276 (2001) 4128-4133
26. Levine J.M., Reynolds R., and Fawcett J.W. The oligodendrocyte precursor cell in health and disease. Trends Neurosci 24 (2001) 39-47
27. Lin W., Jing N., Basson M.A., Dierich A., Licht J., and Ang S.L. Synergistic activity of Sef and Sprouty proteins in regulating the expression of Gbx2 in the mid-hindbrain region. Genesis 41 (2005) 110-115
28. Madsen T.M., Treschow A., Bengzon J., Bolwig T.G., Lindvall O., and Tingstrom A. Increased neurogenesis in a model of electroconvulsive therapy. Biol Psychiatry 47 (2000) 1043-1049
29. Madsen T.M., Yeh D.D., Valentine G.W., and Duman R.S. Electroconvulsive seizure treatment increases cell proliferation in rat frontal cortex. Neuropsychopharmacology 30 (2005) 27-34
30. Mandyam C.D., Norris R.D., and Eisch A.J. Chronic morphine induces premature mitosis of proliferating cells in the adult mouse subgranular zone. J Neurosci Res 76 (2004) 783-794
31. Mayberg H.S. Limbic-cortical dysregulation: a proposed model of depression. J Neuropsychiatry Clin Neurosci 9 (1997) 471-481
32. Michael N., Erfurth A., Ohrmann P., Arolt V., Heindel W., and Pfleiderer B. Neurotrophic effects of electroconvulsive therapy: a proton magnetic resonance study of the left amygdalar region in patients with treatment-resistant depression. Neuropsychopharmacology 28 (2003) 720-725
33. Milad M.R., and Quirk G.J. Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420 (2002) 70-74
34. Minowada G., and Miller Y.E. Sprouty 2 gene in mouse lung tumorigenesis. Chest 125 (2004) 111S
35. Monje M.L., Mizumatsu S., Fike J.R., and Palmer T.D. Irradiation induces neural precursor-cell dysfunction. Nat Med 8 (2002) 955-962
36. Nibuya M., Morinobu S., and Duman R.S. Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J Neurosci 15 (1995) 7539-7547
37. Obergriesser T., Ende G., Braus D.F., and Henn F.A. Long-term follow-up of magnetic resonance-detectable choline signal changes in the hippocampus of patients treated with electroconvulsive therapy. J Clin Psychiatry 64 (2003) 775-780
38. Öngür D., Drevets W.C., and Price J.L. Glial reduction in the subgenual prefrontal cortex in mood disorders. Proc Natl Acad Sci U S A 95 (1998) 13290-13295
39. Öngür D., and Price J.L. The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10 (2000) 206-219
40. Overstreet L.S. Quantal transmission: not just for neurons. Trends Neurosci 28 (2005) 59-62
41. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates. Third ed. (1997), Academic Press, San Diego, CA
42. Pohlman J.M., Ongur D., Eisch A.J., Edwin F., Heckers S., Cohen B.M., et al. Electroconvulsive seizures stimulate cellular proliferation and reduce expression of Sprouty2 within the prefrontal cortex of rats. Society for Neuroscience 31 (2005) 1024-1028
43. Poppleton H.M., Edwin F., Jaggar L., Ray R., Johnson L.R., and Patel T.B. Sprouty regulates cell migration by inhibiting the activation of Rac1 GTPase. Biochem Biophys Res Commun 323 (2004) 98-103
44. Prudic J., Haskett R.F., Mulsant B., Malone K.M., Pettinati H.M., Stephens S., et al. Resistance to antidepressant medications and short-term clinical response to ECT. Am J Psychiatry 153 (1996) 985-992
45. Rankin S.L., Partlow G.D., McCurdy R.D., Giles E.D., and Fisher K.R. The use of proliferating cell nuclear antigen immunohistochemistry with a unique functional marker to detect postnatal neurogenesis in paraffin-embedded sections of the mature pig brain. Brain Res Brain Res Protoc 13 (2004) 69-75
46. Rubin C., Litvak V., Medvedovsky H., Zwang Y., Lev S., and Yarden Y. Sprouty fine-tunes EGF signaling through interlinked positive and negative feedback loops. Curr Biol 13 (2003) 297-307
47. Sackeim H.A., Haskett R.F., Mulsant B.H., Thase M.E., Mann J.J., Pettinati H.M., et al. Continuation pharmacotherapy in the prevention of relapse following electroconvulsive therapy: a randomized controlled trial. JAMA 285 (2001) 1299-1307
48. Scott B.W., Wojtowicz J.M., and Burnham W.M. Neurogenesis in the dentate gyrus of the rat following electroconvulsive shock seizures. Exp Neurol 165 (2000) 231-236
49. Smith M.A., Zhang L.X., Lyons W.E., and Mamounas L.A. Anterograde transport of endogenous brain-derived neurotrophic factor in hippocampal mossy fibers. Neuroreport 8 (1997) 1829-1834
50. Toschi L., and Bravo R. Changes in cyclin/proliferating cell nuclear antigen distribution during DNA repair synthesis. J Cell Biol 107 (1988) 1623-1628
51. UK-ECT-Review-Group. Efficacy and safety of electroconvulsive therapy in depressive disorders: a systematic review and meta-analysis. Lancet 361 (2003) 799-808
52. Vaidya V.A., Siuciak J.A., Du F., and Duman R.S. Hippocampal mossy fiber sprouting induced by chronic electroconvulsive seizures. Neuroscience 89 (1999) 157-166
53. Wennstrom M., Hellsten J., Ekdahl C.T., and Tingstrom A. Electroconvulsive seizures induce proliferation of NG2-expressing glial cells in adult rat hippocampus. Biol Psychiatry 54 (2003) 1015-1024
54. Wennstrom M., Hellsten J., and Tingstrom A. Electroconvulsive seizures induce proliferation of NG2-expressing glial cells in adult rat amygdala. Biol Psychiatry 55 (2004) 464-471
55. Yigzaw Y., Cartin L., Pierre S., Scholich K., and Patel T.B. The C terminus of sprouty is important for modulation of cellular migration and proliferation. J Biol Chem 276 (2001) 22742-22747
56. Yigzaw Y., Poppleton H.M., Sreejayan N., Hassid A., and Patel T.B. Protein-tyrosine phosphatase-1B (PTP1B) mediates the anti-migratory actions of Sprouty. J Biol Chem 278 (2003) 284-288
57. Zhang C., Chaturvedi D., Jaggar L., Magnuson D., Lee J.M., and Patel T.B. Regulation of vascular smooth muscle cell proliferation and migration by human sprouty 2. Arterioscler Thromb Vasc Biol 25 (2005) 533-538