Chronic lithium treatment decreases NG2 cell proliferation in rat dentate hilus, amygdala and corpus callosum

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 33, Issue 3, 2009, Pages 503-510

  Orre, Karin ^a   Wennström, Malin ^a   Tingström, Anders ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

Amygdala; Bipolar disorder; Corpus callosum; Hippocampus; Lithium; NG2 cells

Indexed keywords

BROXURIDINE; LITHIUM; PROTEOCHONDROITIN SULFATE; PROTEOCHONDROITIN SULFATE NG 2; UNCLASSIFIED DRUG;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIPOLAR DISORDER; CELL FUNCTION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CORPUS CALLOSUM; DENTATE GYRUS; DRUG ACTIVITY; DRUG BLOOD LEVEL; DRUG DOSE REDUCTION; GLIA CELL; IMMUNOHISTOCHEMISTRY; MALE; NG 2 CELL; NONHUMAN; OLIGODENDROGLIA; RAT; TREATMENT DURATION; WISTAR RAT;

ADENOMATOUS POLYPOSIS COLI; AMYGDALA; ANIMALS; ANTIGENS; ANTIPSYCHOTIC AGENTS; BROMODEOXYURIDINE; CELL COUNT; CELL PROLIFERATION; CORPUS CALLOSUM; DENTATE GYRUS; DRUG ADMINISTRATION SCHEDULE; KI-67 ANTIGEN; LITHIUM CHLORIDE; MALE; NEURONS; OLIGODENDROGLIA; PROTEOGLYCANS; RATS; RATS, WISTAR; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES;

EID: 62849111262     PISSN: 02785846     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2009.01.015     Document Type: Article

References (85)

1. Adamo A.M., Paez P.M., Escobar Cabrera O.E., Wolfson M., Franco P.G., Pasquini J.M., et al. Remyelination after cuprizone-induced demyelination in the rat is stimulated by apotransferrin. Exp Neurol 198 2 (2006) 519-529
2. Antonelli T., Ferioli V., Lo Gallo G., Tomasini M.C., Fernandez M., O'Connor W.T., et al. Differential effects of acute and short-term lithium administration on dialysate glutamate and GABA levels in the frontal cortex of the conscious rat. Synapse 38 3 (2000) 355-362
3. Bachmann R.F., Schloesser R.J., Gould T.D., and Manji H.K. Mood stabilizers target cellular plasticity and resilience cascades: implications for the development of novel therapeutics. Mol Neurobiol 32 2 (2005) 173-202
4. Barres B.A., and Raff M.C. Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons. Nature 361 6409 (1993) 258-260
5. Bergles D.E., Roberts J.D., Somogyi P., and Jahr C.E. Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405 6783 (2000) 187-191
6. Beyer J.L., Kuchibhatla M., Payne M.E., Moo-Young M., Cassidy F., Macfall J., et al. Hippocampal volume measurement in older adults with bipolar disorder. Am J Geriatr Psychiatry 12 6 (2004) 613-620
7. Bhat R.V., Axt K.J., Fosnaugh J.S., Smith K.J., Johnson K.A., Hill D.E., et al. Expression of the APC tumor suppressor protein in oligodendroglia. Glia 17 2 (1996) 169-174
8. Blumberg H.P., Kaufman J., Martin A., Whiteman R., Zhang J.H., Gore J.C., et al. Amygdala and hippocampal volumes in adolescents and adults with bipolar disorder. Arch Gen Psychiatry 60 12 (2003) 1201-1208
9. Bowley M.P., Drevets W.C., Ongur D., and Price J.L. Low glial numbers in the amygdala in major depressive disorder. Biol Psychiatry 52 5 (2002) 404-412
10. Brambilla P., Glahn D.C., Balestrieri M., and Soares J.C. Magnetic resonance findings in bipolar disorder. Psychiatr Clin North Am 28 2 (2005) 443-467
11. Brambilla P., Harenski K., Nicoletti M., Sassi R.B., Mallinger A.G., Frank E., et al. MRI investigation of temporal lobe structures in bipolar patients. J Psychiatr Res 37 4 (2003) 287-295
12. Brambilla P., Nicoletti M., Sassi R.B., Mallinger A.G., Frank E., Keshavan M.S., et al. Corpus callosum signal intensity in patients with bipolar and unipolar disorder. J Neurol Neurosurg Psychiatry 75 2 (2004) 221-225
13. Brambilla P., Nicoletti M.A., Sassi R.B., Mallinger A.G., Frank E., Kupfer D.J., et al. Magnetic resonance imaging study of corpus callosum abnormalities in patients with bipolar disorder. Biol Psychiatry 54 11 (2003) 1294-1297
14. Bu J., Banki A., Wu Q., and Nishiyama A. Increased NG2(+) glial cell proliferation and oligodendrocyte generation in the hypomyelinating mutant shiverer. Glia 48 1 (2004) 51-63
15. Butt A.M., Hamilton N., Hubbard P., Pugh M., and Ibrahim M. Synantocytes: the fifth element. J Anat 207 6 (2005) 695-706
16. Caetano S.C., Silveira C.M., Kaur S., Nicoletti M., Hatch J.P., Brambilla P., et al. Abnormal corpus callosum myelination in pediatric bipolar patients. J Affect Disord 108 3 (2008) 297-301
17. Chambers J.S., and Perrone-Bizzozero N.I. Altered myelination of the hippocampal formation in subjects with schizophrenia and bipolar disorder. Neurochem Res 29 12 (2004) 2293-2302
18. Chen G., Rajkowska G., Du F., Seraji-Bozorgzad N., and Manji H.K. Enhancement of hippocampal neurogenesis by lithium. J Neurochem 75 4 (2000) 1729-1734
19. Chuang D.M., Chen R.W., Chalecka-Franaszek E., Ren M., Hashimoto R., Senatorov V., et al. Neuroprotective effects of lithium in cultured cells and animal models of diseases. Bipolar Disord 4 2 (2002) 129-136
20. Cooper-Kuhn C.M., and Kuhn H.G. Is it all DNA repair? Methodological considerations for detecting neurogenesis in the adult brain. Brain Res Dev Brain Res 134 1-2 (2002) 13-21
21. Dawson M.R., Polito A., Levine J.M., and Reynolds R. NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS. Mol Cell Neurosci 24 2 (2003) 476-488
22. Di Bello I.C., Dawson M.R., Levine J.M., and Reynolds R. Generation of oligodendroglial progenitors in acute inflammatory demyelinating lesions of the rat brain stem is associated with demyelination rather than inflammation. J Neurocytol 28 4-5 (1999) 365-381
23. Dixon J.F., and Hokin L.E. Lithium acutely inhibits and chronically up-regulates and stabilizes glutamate uptake by presynaptic nerve endings in mouse cerebral cortex. Proc Natl Acad Sci U S A 95 14 (1998) 8363-8368
24. Drevets W.C., Price J.L., Simpson Jr. J.R., Todd R.D., Reich T., Vannier M., et al. Subgenual prefrontal cortex abnormalities in mood disorders. Nature 386 6627 (1997) 824-827
25. Du J., Creson T.K., Wu L.J., Ren M., Gray N.A., Falke C., et al. The role of hippocampal GluR1 and GluR2 receptors in manic-like behavior. J Neurosci 28 1 (2008) 68-79
26. Frangou S. The Maudsley Bipolar Disorder Project. Epilepsia 46 Suppl 4 (2005) 19-25
27. Friedman B., Hockfield S., Black J.A., Woodruff K.A., and Waxman S.G. In situ demonstration of mature oligodendrocytes and their processes: an immunocytochemical study with a new monoclonal antibody, rip. Glia 2 5 (1989) 380-390
28. Friedman S.D., Dager S.R., Parow A., Hirashima F., Demopulos C., Stoll A.L., et al. Lithium and valproic acid treatment effects on brain chemistry in bipolar disorder. Biol Psychiatry 56 5 (2004) 340-348
29. Gallo V., Mangin J.M., Kukley M., and Dietrich D. Synapses on NG2-expressing progenitors in the brain: multiple functions?. J Physiol 586 16 (2008) 3767-3781
30. Gottesfeld Z. Effect of lithium and other alkali metals on brain chemistry and behavior. I. Glutamic acid and GABA in brain regions. Psychopharmacologia 45 3 (1976) 239-242
31. Gundersen H.J., Jensen E.B., Kieu K., and Nielsen J. The efficiency of systematic sampling in stereology-reconsidered. J Microsc 193 Pt 3 (1999) 199-211
32. Hampton D.W., Rhodes K.E., Zhao C., Franklin R.J., and Fawcett J.W. The responses of oligodendrocyte precursor cells, astrocytes and microglia to a cortical stab injury, in the brain. Neuroscience 127 4 (2004) 813-820
33. Harrison P.J. The neuropathology of primary mood disorder. Brain 125 Pt 7 (2002) 1428-1449
34. Hashimoto K., Sawa A., and Iyo M. Increased levels of glutamate in brains from patients with mood disorders. Biol Psychiatry 62 11 (2007) 1310-1316
35. Hashimoto R., Senatorov V., Kanai H., Leeds P., and Chuang D.M. Lithium stimulates progenitor proliferation in cultured brain neurons. Neuroscience 117 1 (2003) 55-61
36. Huang J.K., Phillips G.R., Roth A.D., Pedraza L., Shan W., Belkaid W., et al. Glial membranes at the node of Ranvier prevent neurite outgrowth. Science 310 5755 (2005) 1813-1817
37. Jablonska B., Aguirre A., Vandenbosch R., Belachew S., Berthet C., Kaldis P., et al. Cdk2 is critical for proliferation and self-renewal of neural progenitor cells in the adult subventricular zone. J Cell Biol 179 6 (2007) 1231-1245
38. Jamison K.R. Suicide and bipolar disorder. J Clin Psychiatry 61 Suppl 9 (2000) 47-51
39. Jones L.L., Yamaguchi Y., Stallcup W.B., and Tuszynski M.H. NG2 is a major chondroitin sulfate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. J Neurosci 22 7 (2002) 2792-2803
40. Karram K., Chatterjee N., and Trotter J. NG2-expressing cells in the nervous system: role of the proteoglycan in migration and glial-neuron interaction. J Anat 207 6 (2005) 735-744
41. Kim J.S., Chang M.Y., Yu I.T., Kim J.H., Lee S.H., Lee Y.S., et al. Lithium selectively increases neuronal differentiation of hippocampal neural progenitor cells both in vitro and in vivo. J Neurochem 89 2 (2004) 324-336
42. Knutson P., Ghiani C.A., Zhou J.M., Gallo V., and McBain C.J. K+ channel expression and cell proliferation are regulated by intracellular sodium and membrane depolarization in oligodendrocyte progenitor cells. J Neurosci 17 8 (1997) 2669-2682
43. Kukley M., Capetillo-Zarate E., and Dietrich D. Vesicular glutamate release from axons in white matter. Nat Neurosci 10 3 (2007) 311-320
44. Levine S., Saltzman A., and Klein A.W. Proliferation of glial cells in vivo induced in the neural lobe of the rat pituitary by lithium. Cell Prolif 33 4 (2000) 203-207
45. Levison S.W., Young G.M., and Goldman J.E. Cycling cells in the adult rat neocortex preferentially generate oligodendroglia. J Neurosci Res 57 4 (1999) 435-446
46. Malberg J.E., Eisch A.J., Nestler E.J., and Duman R.S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20 24 (2000) 9104-9110
47. Marcus S.R., Nadiger H.A., Chandrakala M.V., Rao T.I., and Sadasivudu B. Acute and short-term effects of lithium on glutamate metabolism in rat brain. Biochem Pharmacol 35 3 (1986) 365-369
48. Meier S., Brauer A.U., Heimrich B., Nitsch R., and Savaskan N.E. Myelination in the hippocampus during development and following lesion. Cell Mol Life Sci 61 9 (2004) 1082-1094
49. Moore G.J., Bebchuk J.M., Wilds I.B., Chen G., and Manji H.K. Lithium-induced increase in human brain grey matter. Lancet 356 9237 (2000) 1241-1242
50. Mork A. Effects of lithium treatment on extracellular serotonin levels in the dorsal hippocampus and wet-dog shakes in the rat. Eur Neuropsychopharmacol 8 4 (1998) 267-272
51. Nishiyama A. Polydendrocytes: NG2 cells with many roles in development and repair of the CNS. Neuroscientist 13 1 (2007) 62-76
52. Noga J.T., Vladar K., and Torrey E.F. A volumetric magnetic resonance imaging study of monozygotic twins discordant for bipolar disorder. Psychiatry Res 106 1 (2001) 25-34
53. Nonaka S., Hough C.J., and Chuang D.M. Chronic lithium treatment robustly protects neurons in the central nervous system against excitotoxicity by inhibiting N-methyl-d-aspartate receptor-mediated calcium influx. Proc Natl Acad Sci U S A 95 5 (1998) 2642-2647
54. Nunez J.L., Nelson J., Pych J.C., Kim J.H., and Juraska J.M. Myelination in the splenium of the corpus callosum in adult male and female rats. Brain Res Dev Brain Res 120 1 (2000) 87-90
55. O'Donnell K.C., and Gould T.D. The behavioral actions of lithium in rodent models: leads to develop novel therapeutics. Neurosci Biobehav Rev 31 6 (2007) 932-962
56. Ohta K., Iwai M., Sato K., Omori N., Nagano I., Shoji M., et al. Dissociative increase of oligodendrocyte progenitor cells between young and aged rats after transient cerebral ischemia. Neurosci Lett 335 3 (2003) 159-162
57. Ong W.Y., and Levine J.M. A light and electron microscopic study of NG2 chondroitin sulfate proteoglycan-positive oligodendrocyte precursor cells in the normal and kainate-lesioned rat hippocampus. Neuroscience 92 1 (1999) 83-95
58. Ongur D., Jensen J.E., Prescot A.P., Stork C., Lundy M., Cohen B.M., et al. Abnormal glutamatergic neurotransmission and neuronal-glial interactions in acute mania. Biol Psychiatry 64 8 (2008) 718-726
59. Pardo R., Andreolotti A.G., Ramos B., Picatoste F., and Claro E. Opposed effects of lithium on the MEK-ERK pathway in neural cells: inhibition in astrocytes and stimulation in neurons by GSK3 independent mechanisms. J Neurochem 87 2 (2003) 417-426
60. Patneau D.K., Wright P.W., Winters C., Mayer M.L., and Gallo V. Glial cells of the oligodendrocyte lineage express both kainate- and AMPA-preferring subtypes of glutamate receptor. Neuron 12 2 (1994) 357-371
61. Paukert M., and Bergles D.E. Synaptic communication between neurons and NG2+ cells. Curr Opin Neurobiol 16 5 (2006) 515-521
62. Paxinos G., and Watson C. The rat brain in stereotactic coordinates (1986), Academic Press Australia, Sydney
63. Pini S., de Queiroz V., Pagnin D., Pezawas L., Angst J., Cassano G.B., et al. Prevalence and burden of bipolar disorders in European countries. Eur Neuropsychopharmacol 15 4 (2005) 425-434
64. Polito A., and Reynolds R. NG2-expressing cells as oligodendrocyte progenitors in the normal and demyelinated adult central nervous system. J Anat 207 6 (2005) 707-716
65. Rajkowska G., Halaris A., and Selemon L.D. Reductions in neuronal and glial density characterize the dorsolateral prefrontal cortex in bipolar disorder. Biol Psychiatry 49 9 (2001) 741-752
66. Rajkowska G., and Miguel-Hidalgo J.J. Gliogenesis and glial pathology in depression. CNS Neurol Disord Drug Targets 6 3 (2007) 219-233
67. Scholzen T., and Gerdes J. The Ki-67 protein: from the known and the unknown. J Cell Physiol 182 3 (2000) 311-322
68. Shibuya-Tayoshi S., Tayoshi S., Sumitani S., Ueno S., Harada M., and Ohmori T. Lithium effects on brain glutamatergic and GABAergic systems of healthy volunteers as measured by proton magnetic resonance spectroscopy. Prog Neuropsychopharmacol Biol Psychiatry 32 1 (2008) 249-256
69. Slomianka L., and West M.J. Estimators of the precision of stereological estimates: an example based on the CA1 pyramidal cell layer of rats. Neuroscience 136 3 (2005) 757-767
70. Stegmuller J., Werner H., Nave K.A., and Trotter J. The proteoglycan NG2 is complexed with alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors by the PDZ glutamate receptor interaction protein (GRIP) in glial progenitor cells. Implications for glial-neuronal signaling. J Biol Chem 278 6 (2003) 3590-3598
71. Strakowski S.M., DelBello M.P., Sax K.W., Zimmerman M.E., Shear P.K., Hawkins J.M., et al. Brain magnetic resonance imaging of structural abnormalities in bipolar disorder. Arch Gen Psychiatry 56 3 (1999) 254-260
72. Swayze II V.W., Andreasen N.C., Alliger R.J., Yuh W.T., and Ehrhardt J.C. Subcortical and temporal structures in affective disorder and schizophrenia: a magnetic resonance imaging study. Biol Psychiatry 31 3 (1992) 221-240
73. Tan A.M., Colletti M., Rorai A.T., Skene J.H., and Levine J.M. Antibodies against the NG2 proteoglycan promote the regeneration of sensory axons within the dorsal columns of the spinal cord. J Neurosci 26 18 (2006) 4729-4739
74. Tan A.M., Zhang W., and Levine J.M. NG2: a component of the glial scar that inhibits axon growth. J Anat 207 6 (2005) 717-725
75. Tanaka K., Nogawa S., Ito D., Suzuki S., Dembo T., Kosakai A., et al. Activation of NG2-positive oligodendrocyte progenitor cells during post-ischemic reperfusion in the rat brain. Neuroreport 12 10 (2001) 2169-2174
76. Tkachev D., Mimmack M.L., Ryan M.M., Wayland M., Freeman T., Jones P.B., et al. Oligodendrocyte dysfunction in schizophrenia and bipolar disorder. Lancet 362 9386 (2003) 798-805
77. Ughrin Y.M., Chen Z.J., and Levine J.M. Multiple regions of the NG2 proteoglycan inhibit neurite growth and induce growth cone collapse. J Neurosci 23 1 (2003) 175-186
78. Vostrikov V.M., Uranova N.A., and Orlovskaya D.D. Deficit of perineuronal oligodendrocytes in the prefrontal cortex in schizophrenia and mood disorders. Schizophr Res 94 1-3 (2007) 273-280
79. Watanabe M., Toyama Y., and Nishiyama A. Differentiation of proliferated NG2-positive glial progenitor cells in a remyelinating lesion. J Neurosci Res 69 6 (2002) 826-836
80. Weissman M.M., Bland R.C., Canino G.J., Faravelli C., Greenwald S., Hwu H.G., et al. Cross-national epidemiology of major depression and bipolar disorder. Jama 276 4 (1996) 293-299
81. Wennstrom M., Hellsten J., and Tingstrom A. Electroconvulsive seizures induce proliferation of NG2-expressing glial cells in adult rat amygdala. Biol Psychiatry 55 5 (2004) 464-471
82. Yang Z., Suzuki R., Daniels S.B., Brunquell C.B., Sala C.J., and Nishiyama A. NG2 glial cells provide a favorable substrate for growing axons. J Neurosci 26 14 (2006) 3829-3839
83. Yuan X., Eisen A.M., McBain C.J., and Gallo V. A role for glutamate and its receptors in the regulation of oligodendrocyte development in cerebellar tissue slices. Development 125 15 (1998) 2901-2914
84. Yucel K., Taylor V.H., McKinnon M.C., Macdonald K., Alda M., Young L.T., et al. Bilateral hippocampal volume increase in patients with bipolar disorder and short-term lithium treatment. Neuropsychopharmacology 33 2 (2008) 361-367
85. Ziskin J.L., Nishiyama A., Rubio M., Fukaya M., and Bergles D.E. Vesicular release of glutamate from unmyelinated axons in white matter. Nat Neurosci 10 3 (2007) 321-330