Lesioning noradrenergic neurons of the locus coeruleus in C57Bl/6 mice with unilateral 6-hydroxydopamine injection, to assess molecular, electrophysiological and biochemical changes in noradrenergic signaling

Neuroscience

Volumn 216, Issue , 2012, Pages 143-157

  Szot, P ^a,b   Knight, L ^c   Franklin, A ^a   Sikkema, C ^a   Foster, S ^c   Wilkinson, C W ^a   White, S S ^a,b   Raskind, M A ^a,b  

^a VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c WHITMAN COLLEGE   (United States)

Author keywords

Dopamine hydroxylase; Frontal cortex; Hippocampus; Norepinephrine transporter; Single unit extracellular electrophysiology; Tyrosine hydroxylase

Indexed keywords

ALPHA 1 ADRENERGIC RECEPTOR; ALPHA 2 ADRENERGIC RECEPTOR; CATECHOLAMINE; DOPAMINE BETA MONOOXYGENASE; MESSENGER RNA; NORADRENALIN TRANSPORTER; OXIDOPAMINE;

ACTION POTENTIAL; AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; BRAIN ELECTROPHYSIOLOGY; CELL LOSS; CELL SURVIVAL; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DOSE RESPONSE; FOREBRAIN; FRONTAL CORTEX; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; LOCUS CERULEUS; MALE; MOUSE; NONHUMAN; NORADRENERGIC NERVE; NORADRENERGIC SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; STEREOTACTIC PROCEDURE; SUBSTANTIA NIGRA; VENTRAL TEGMENTUM;

ADRENERGIC AGENTS; ADRENERGIC NEURONS; ANIMALS; BEHAVIOR, ANIMAL; BRAIN MAPPING; DISEASE MODELS, ANIMAL; DOPAMINERGIC NEURONS; ELECTROPHYSIOLOGICAL PHENOMENA; HIPPOCAMPUS; LOCUS COERULEUS; MALE; MICE; MICE, INBRED C57BL; NOREPINEPHRINE; OXIDOPAMINE; RNA, MESSENGER; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA;

EID: 84862019744     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.04.046     Document Type: Article

References (72)

1. Adolfsson R., Gottfries C.G., Roos B.E., Winblad B. Changes in the brain catecholamines in patients with dementia of Alzheimer's type. Br J Psychiatry 1979, 135:216-223.
2. Aghajanian G.K., VanderMaelen C.P. α2-Adrenoreceptor-mediated hyperpolarization of locus coeruleus neurons; intracellular studies in vivo. Science 1982, 215:1394-1396.
3. Antelman S.M., Caggiula A.R. Norepinephrine-dopamine interaction and behavior. Science 1977, 195:646-653.
4. Aston-Jones G., Rajkowski J., Cohen J. Role of locus coeruleus in attention and behavioral flexibility. Biol Psychiatry 1999, 46:1309-1320.
5. Bertrand E., Lechowicz W., Szpak G.M., Dynecki J. Qualitative and quantitative analysis of locus coeruleus neurons in Parkinson's disease. Folia Neuropathol 1997, 35:80-86.
6. 2 drive to breathing. Pflugers Arch Eur J Physiol 2008, 455:1119-1128.
7. Bondareff W., Mountjoy C.Q., Roth M. Selective loss of neurons of origin of adrenergic projection to cerebral cortex (nucleus locus coeruleus) in senile dementia. Lancet 1981, 1:783-784.
8. Booze R.M., Hall J.A., Cress N.M., Miller G.D., Davis J.N. DESP-4 treatment produces abnormal tyrosine hydroxylase immunoreactive fibers in rat hippocampus. Exp Neural 1988, 101:75-86.
9. Cash R., Dennis T., L'Heureux R., Raisman R., Javoy-Agid F., Scatton B. Parkinson's disease and dementia: norepinephrine and dopamine in locus coeruleus. Neurology 1987, 37:42-46.
10. Chan-Palay V., Asan E. Alterations in catecholamine neurons of the locus coeruleus in senile dementia of the Alzheimer's type and in Parkinson's disease with and without dementia and depression. J Comp Neurol 1989, 287:373-392.
11. Chan-Palay V., Asan E. Alterations in the locus coeruleus in dementias of Alzheimer's and Parkinson's disease. Prog Brain Res 1991, 88:625-630.
12. Cheetham S.C., Viggers J.A., Butler S.A., Prow M.R., Heal D.J. [3H]Nisoxetine - a radioligand for noradrenaline reuptake sites: correlation with inhibition of [3H]noradrenaline uptake and effect of DSP-4 lesioning and antidepressant treatment. Neuropharmacology 1996, 35:63-70.
13. Coradazzi M., Gulino R., Garozzo S., Leanza G. Selective lesion of the developing central noradrenergic system: short- and long-term effects and reinnervation by noradrenergic-rich tissue grafts. J Neurochem 2010, 114:761-771.
14. Cross A.J., Crow T.J., Perry E.K., Perry R.H., Blessed G., Tomlinson B.E. Reduced dopamine-beta-hydroxylase activity in Alzheimer's disease. BMJ (Clin Res Ed) 1981, 282:93-94.
15. Descarries L., Saucier G. Disappearance of the locus coeruleus in the rat after intraventricular 6-hydroxydopamine. Brain Res 1972, 37:310-316.
16. Eisenhofer G., Goldstein D.S., Stull R., Kelser H.R., Sunderland T., Murphy D.L., Koplin I.J. Simultaneous liquid-chromatographic determination of 3,4-dihydroxyphenylglycol, catecholamines, and 3,4-dihydroxyphenylalanine in plasma, and their response to inhibition of monoamine oxidase. Clin Chem 1986, 32:2030-2033.
17. Fitzgerald P.J. Is elevated norepinephrine an etiological factor in some cases of Alzheimer's disease?. Curr Alzheimer's Res 2010, 7:506-516.
18. Gasper P., Duyckaerts C., Alvarez C., Javoy-Agid F., Berger B. Alterations of dopaminergic and noradrenergic innervation in motor cortex in Parkinson's disease. Ann Neurol 1991, 30:365-374.
19. Gasper P., Gray F. Parkinson's disease: a neuropathological study of 32 cases. Acta Neuropathol 1984, 64:43-52.
20. German D.C., Manaye K.F., White C.L., Woodward D.J., McIntyre D.D., Smith W.K., Kalaria R.N., Mann D.M. Disease-specific patterns of locus coeruleus cell loss. Ann Neurol 1992, 32:667-676.
21. Grima B., Lamouroux A., Blanot F., Biguet N.F., Mallet J. Complete coding sequence of rat tyrosine hydroxylase mRNA. Proc Natl Acad Sci USA 1985, 82:617-621.
22. Grzanna R., Berger U., Fritschy J.-M., Geffard M. Acute action of DSP-4 on central norepinephrine axons: biochemical and immunohistochemical evidence for differential effects. J Histochem Cytochem 1989, 37:1435-1442.
23. Guiard B.P., Mansari M.E., Merali Z., Blier P. Functional interactions between dopamine, serotonin and norepinephrine neurons: an in-vivo electrophysiological study in rats with monoaminergic lesions. Int J Neuropsychopharm 2008, 11:625-639.
24. Harik S. Locus ceruleus lesion by local 6-hydroxydopamine infusion causes marked and specific destruction of noradrenergic neurons, long-term depletion of norepinephrine and the enzymes that synthesize it, and enhanced dopaminergic mechanisms in the ipsilateral cerebral cortex. J Neurosci 1984, 4:699-707.
25. Henderson G., Pepper C.M., Shefner S.A. Electrophysiological properties of neurons contained in the locus coeruleus and mesencephalic nucleus of the trigeminal nerve in vitro. Exp Brain Res 1982, 45:29-37.
26. Hoogendijk W.J., Freenstra M.G., Botterblom M.H., Gilhuis J., Sommer I.E., Kamphorst W., Eikelenboom P., Swaab D.F. Increased activity of surviving locus coeruleus neurons in Alzheimer's disease. Ann Neurol 1999, 45:82-91.
27. Hughes Z.A., Stanford S.C. A partial noradrenergic lesion induced by DSP-4 increases extracellular noradrenaline concentration in rat frontal cortex: a microdialysis study in vivo. Psychopharmacology 1998, 136:299-303.
28. Iversen L.L., Iversen S.D., Bloom F.E., Roth R.H. Introduction to neuropsychopharmacology 2009, pp 150-213, Oxford University Press, New York, NY.
29. Jonsson G., Hallman H., Ponzio F., Ross S. DSP4 (N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine) - a useful denervation tool for central and peripheral noradrenaline neurons. Eur J Pharmacol 1981, 72:173-188.
30. Kask A., Harro J., Tuomainen P., Rago L., Mannisto P.T. Overflow of noradrenaline and dopamine in frontal cortex after [N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine] (DSP-4) treatment: in vivo microdialysis study in anaesthetized rats. Naunyn Schmiedeberg's Arch Pharmacol 1997, 355:267-272.
31. Kish S.J., Shannak K.S., Rajput A.H., Gilbert J.J., Hornykiewicz O. Cerebellar norepinephrine in patients with Parkinson's disease and control subjects. Arch Neurol 1984, 41:612-614.
32. Kitt C.A., Brauth S.E. Telencephalic projections from midbrain and isthmal cell groups in the pigeon. I. Locus coeruleus and subcoeruleus. J Comp Neurol 1986, 247:69-91.
33. L'Heureux R., Dennis T., Curet O., Scatton B. Measurement of endogenous noradrenaline release in the cerebral cortex in vivo by transcortical dialysis: effects of drugs affecting noradrenergic transmission. J Neurochem 1986, 46:1794-1801.
34. Lindvall O., Bjorklund A. The organization of the ascending catecholamine neuron systems in the rat brain as revealed by the glyoxylic acid fluorescence method. Acta Physiol Scand Suppl 1974, 412:1-48.
35. Loughlin S.E., Foote S.L., Bloom F.E. Efferent projections of nucleus locus coeruleus: topographic organization of cells of origin demonstrated by three-dimensional reconstruction. Neuroscience 1986, 18:291-306.
36. Loughlin S.E., Foote S.L., Grzanna R. Efferent projections of nucleus locus coeruleus noradrenaline neurons: morphologic subpopulations have different efferent's targets. Neuroscience 1986, 18:307-319.
37. Lyons W.E., Fritschy J.M., Grzanna R. The noradrenergic neurotoxin DSP-4 eliminates the coerulespinal projection but spares projections of the A5 and A7 groups to the ventral horn of the rat spinal cord. J Neurosci 1989, 9:1481-1489.
38. Mann J.J., Stanley M., Neophytides A., deLeon M.J., Ferris S.H., Gershon S. Central amine metabolism in Alzheimer's disease: in vivo relationship to cognitive deficit. Neurobiol Aging 1981, 2:57-60.
39. Marcyniuk B., Mann D.M., Yates P.O. Loss of nerve cells from locus coeruleus in Alzheimer's disease is topographically arranged. Neurosci Lett 1986, 64:247-252.
40. Mason S.T., Fibiger H.D. Regional topography within noradrenergic locus coeruleus as revealed by retrograde transport of horseradish peroxidase. J Comp Neurol 1979, 187:703-724.
41. Matsukawa M., Nakadate K., Ishihara I., Okado N. Synaptic loss following depletion of noradrenaline and/or serotonin in the rat visual cortex: a quantitative electron microscopic study. Neuroscience 2003, 122:627-635.
42. McBride R.L., Sutin J. Projections of the locus coeruleus and adjacent pontine tegmentum in the cat. J Comp Neurol 1976, 165:265-284.
43. McGaugh J.L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 2004, 27:1-28.
44. McMahon A., Geertman R., Sabban E.L. Rat dopamine β-hydroxylase: molecular cloning and characterization of the cDNA and regulation of the mRNA by reserpine. J Neurosci Res 1990, 25:395-404.
45. McMillan P.J., White S.S., Franklin A., Greenup J.L., Leverenz J.B., Raskind M.A., Szot P. Differential response of the central noradrenergic nervous system to the loss of locus coerlues neurons in Parkinson's disease and Alzheimer's disease. Brain Res 2011, 1373:240-252.
46. Moore R.Y., Bloom F.E. Central catecholamine neuron system: anatomy and physiology of the norepinephrine and epinephrine systems. Ann Rev Neurosci 1979, 2:113-168.
47. Olson V.G., Rockett H.R., Reh R., Redila V.A., Tran P.M., Venkov H.A., DeFino M.C., Hague C., Peskind E.R., Szot P., Raskind M.A. The role of norepinephrine in differential response to stress in an animal model of posttraumatic stress disorder. Biol Psychiatry 2011, 70:441-448.
48. Palmer A.M., Wilcock G.K., Esiri M.M., Francis P.T., Bowen D.M. Monoaminergic innervation of the frontal and temporal lobes in Alzheimer's disease. Brain Res 1987, 401:231-238.
49. Patt S., Gerhard L. A Golgi study of human locus coeruleus in normal brains and in Parkinson's disease. Neurpoathol Appl Neurobiol 1993, 19:519-523.
50. Perry E.K., Blessed G., Tomlinson B.E., Perry R.H., Crow T.J., Cross A.J., Dockray G.J., Dimaline R., Arregui A. Neurochemical activities in human temporal lobe related to aging and Alzheimer's-type changes. Neurobiol Aging 1981, 2:251-256.
51. Ressler K.J., Nemeroff C.B. Role of serotonergic and noradrenergic systems in the pathophysiology of depression and anxiety disorders. Depression Anxiety 2000, 12(Suppl 1):2-19.
52. Robertson G.B., Fluharty S.J., Zigmond M.J., Sciabassi R.J., Berger T.W. Recovery of hippocampal dentate granule cell responsiveness to entorhinal cortical input following norepinephrine depletion. Brain Res 1993, 614:21-28.
53. Rommelfanger K.S., Edwards G.L., Freeman K.G., Liles L.C., Miller G.W., Weinshenker D. Norepinephrine loss produces more profound motor deficits than MPTP treatment in mice. Proc Natl Acad Sci 2007, 104:1530-1540.
54. Ross S.B. Long-term effects of N-2-chlorethyl-N-ethyl-2-bromobenzylamine hydrochloride on noradrenergic neurons in the rat brain and heart. Br J Pharmacol 1976, 58:521-527.
55. Russo-Neustadt A., Zomorodian T.J., Cotman C.W. Preserved cerebellar tyrosine hydroxylase-immunoreactive neuronal fibers in a behaviorally aggressive subgroup of Alzheimer's disease patients. Neuroscience 1998, 87:55-61.
56. Sanders J.D., Szot P., Weinshenker D., Happe H.K., Bylund D.B., Murrin L.C. Analysis of brain adrenergic receptors in dopamine-β-hydroxylase knockout mice. Brain Res 2006, 1109:45-53.
57. Shannak K., Rajput A., Rozdilsky B., Kish S., Gilbert J., Hornykiewicz O. Noradrenaline, dopamine and serotonin levels and metabolism in the human hypothalamus: observations in Parkinson's disease and normal subjects. Brain Res 1994, 639:33-41.
58. Southwick S.M., Bremner J.D., Rasmusson A., Morgan C.A., Arnsten A., Charney D.S. Role of norepinephrine in the pathophysiology and treatment of posttraumatic stress disorder. Biol Psychiatry 1999, 46:1192-1204.
59. Strawn J.R., Geracioti T.D. Noradrenergic dysfunction and the psychopharmacology of posttraumatic stress disorder. Depress Anxiety 2008, 25:260-271.
60. Swanson L.W., Hartman B.K. The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine β-hydroxylase as a marker. J Comp Neurol 1975, 163:467-505.
61. Szot P., Miguelez C., White S.S., Franklin A., Sikkema C., Wilkinson C.W., Ugedo L., Raskind M.A. A comprehensive analysis of the effect of DSP4 on the locus coeruleus noradrenergic system in the rat. Neuroscience 2010, 166:279-291.
62. Szot P., Weinshenker D., White S.S., Robbins C.A., Rust N.C., Schwartzkroin P.A., Palmiter R.D. Norepinephrine-deficient mice have increased susceptibility to seizure-inducing stimuli. J Neurosci 1999, 19:10985-10992.
63. Szot P., White S.S., Greenup J.L., Leverenz J.B., Peskind E.R., Raskind M.A. Compensatory changes in the noradrenergic nervous system in the locus coeruleus and hippocampus of postmortem subjects with Alzheimer's disease and dementia with Lewy bodies. J Neurosci 2006, 26:467-478.
64. Szot P., White S.S., Veith R.C. Effect of pentylenetetrazol on the expression of tyrosine hydroxylase mRNA and norepinephrine and dopamine transporter mRNA. Mol Brain Res 1997, 44:46-54.
65. Theron C.N., de Villiers A.S., Taljaard J.J. Effects of DSP-4 on monoamine and monoamine metabolites levels and on beta adrenoreceptor binding kinetics in rat brain at different times after administration. Neurochem Res 1993, 18:1321-1327.
66. Tomlinson B.E., Irving D., Blessed G. Cell loss in the locus coeruleus in senile dementia of the Alzheimer's type. J Neurol Sci 1981, 49:419-428.
67. Wang Y., Zhang Q.J., Liu J., Ali U., Gui Z.H., Hui Y.P., Chen L., Wu Z.H., Li Q. Noradrenergic lesion of the locus coeruleus increases apomorphine-induced circling behavior and the firing activity of substantia nigra pars reticulate neurons in a rat model of Parkinson's disease. Brain Res 2010, 1310:189-199.
68. Weinshenker D., Szot P. The role of catecholamines in seizure susceptibility: new results using genetically engineered mice. Pharmacol Therap 2002, 94:213-233.
69. Weinshenker D., White S.S., Javors M.A., Palmiter R.D., Szot P. Regulation of norepinephrine transporter abundance by catecholamines and desipramine in vivo. Brain Res 2002, 946:239-246.
70. Williams J.T., North R.A., Shefner S.A., Nishi S., Egan T.M. Membrane properties of rat locus coeruleus neurons. Neuroscience 1984, 13:137-156.
71. Wolfman C., Abo V., Calvo D., Medina J., Dajas F., Silveiro R. Recovery of central noradrenergic neurons one year after the administration of the neurotoxin DSP4. Neurochem Int 1994, 25:395-400.
72. Zarow C., Lyness S.A., Mortimer J.A., Chui H.C. Neuronal loss is greater in the locus coeruleus than nucleus basalis and substantia nigra in Alzheimer and Parkinson disease. Arch Neurol 2003, 60:337-341.