Effects of DSP4 on the noradrenergic phenotypes and its potential molecular mechanisms in SH-SY5Y cells

Neurotoxicity Research

Volumn 25, Issue 2, 2014, Pages 193-207

  Wang, Yan ^a   Musich, Phillip R ^a   Serrano, Moises A ^a   Zou, Yue ^a   Zhang, Jia ^a   Zhu, Meng Yang ^a  

^a East Tennessee State University   (United States)

Author keywords

Cell cycle; Degeneration; DNA damage; Dopamine hydroxylase; Neurotoxin; Norepinephrine transporter

Indexed keywords

2 BROMO N (2 CHLOROETHYL) N ETHYLBENZYLAMINE; DOPAMINE BETA MONOOXYGENASE; HISTONE H2AX; MESSENGER RNA; NORADRENALIN; NORADRENALIN TRANSPORTER; PROTEIN P53; SINGLE STRANDED DNA;

ARTICLE; CELL CYCLE ARREST; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; DOWN REGULATION; ENZYME MECHANISM; FLOW CYTOMETER; HUMAN; HUMAN CELL; NEUROBLASTOMA; NORADRENERGIC SYSTEM; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; S PHASE CELL CYCLE CHECKPOINT; SINGLE STRANDED DNA BREAK;

ANIMALIA;

ADRENERGIC AGENTS; BENZYLAMINES; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; DNA DAMAGE; DOPAMINE BETA-HYDROXYLASE; DOWN-REGULATION; HUMANS; NOREPINEPHRINE PLASMA MEMBRANE TRANSPORT PROTEINS; SIGNAL TRANSDUCTION;

EID: 84891850150     PISSN: 10298428     EISSN: 14763524     Source Type: Journal    
DOI: 10.1007/s12640-013-9421-4     Document Type: Article

References (85)

1. Abraham RT (2001) Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev 15:2177-2196 (Pubitemid 32843830)
2. Adamec E, Vonsattel JP, Nixon RA (1999) DNA strand breaks in Alzheimer's disease. Brain Res 849:67-77
3. Anne SL, Saudou F, Humbert S (2007) Phosphorylation of huntingtin by cyclin-dependent kinase 5 is induced by DNA damage and regulates wild-type and mutant huntingtin toxicity in neurons. J Neurosci 27:7318-7328 (Pubitemid 47037570)
4. Axelrod J, Kopin IJ (1969) The uptake, storage, release and metabolism of noradrenaline in sympathetic nerves. Prog Brain Res 31:21-32
5. Bakkenist CJ, Kastan MB (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421:499-506 (Pubitemid 36168436)
6. Bakkenist CJ, Kastan MB (2004) Initiating cellular stress responses. Cell 118:9-17 (Pubitemid 38902810)
7. Barker E, Blakely R (1995) Norepinephrine and serotonin transporters. Molecular targets of antidepressant drugs. In: Bloom F, Kupfer D (eds) Psychopharmacology. A fourth generation of progress. Raven Press, New York, pp 321-333
8. Bartek J, Lukas J (2001) Mammalian G1- and S-phase checkpoints in response to DNA damage. Curr Opin Cell Biol 13:738-747 (Pubitemid 33042735)
9. Biedler JL, Roffler-Tarlov S, Schachner M, Freedman LS (1978) Multiple neurotransmitter synthesis by human neuroblastoma cell lines and clones. Cancer Res 38:3751-3757 (Pubitemid 9045201)
10. Boksa P, Aitken D, Meaney M (1989) Effects of the catecholaminergic neurotoxin N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine (DSP-4) on adrenal chromaffin cells in culture. Biochem Pharmacol 38:1491-1498 (Pubitemid 19123341)
11. Bondareff W, Mountjoy CQ, Roth M (1982) Loss of neurons of origin of the adrenergic projection to cerebral cortex (nucleus locus coeruleus) in senile dementia. Neurology 32:164-168 (Pubitemid 12223999)
12. Burma S, Chen BP, Murphy M, Kurimasa A, Chen DJ (2001) ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J Biol Chem 276:42462-42467 (Pubitemid 37371158)
13. Caldecott KW (2004) DNA single-strand breaks and neurodegeneration. DNA Repair (Amst) 3:875-882 (Pubitemid 38997929)
14. Chan-Palay V, Asan E (1989) Quantitation of catecholamine neurons in the locus coeruleus in human brains of normal young and older adults and in depression. J Comp Neurol 287:357-372 (Pubitemid 19239068)
15. Cho YJ, Liang P (2011) S-phase-coupled apoptosis in tumor suppression. Cell Mol Life Sci 68:1883-1896
16. Del Bino G, Bruno S, Yi PN, Darzynkiewicz Z (1992) Apoptotic cell death triggered by camptothecin or teniposide. The cell cycle specificity and effects of ionizing radiation. Cell Prolif 25:537-548
17. Dooley DJ, Heal DJ, Goodwin GM (1987) Repeated electroconvulsive shock prevents increased neocortical beta 1-adrenoceptor binding after DSP-4 treatment in rats. Eur J Pharmacol 134:333-337 (Pubitemid 17033940)
18. Dudley MW, Howard BD, Cho AK (1990) The interaction of the beta-haloethyl benzylamines, xylamine, and DSP-4 with catecholaminergic neurons. Annu Rev Pharmacol Toxicol 30:387-403
19. Engler H, Doenlen R, Riether C, Engler A, Besedovsky HO, Del Rey A, Pacheco-Lopez G, Schedlowski M (2010) Chemical destruction of brain noradrenergic neurons affects splenic cytokine production. J Neuroimmunol 219:75-80
20. Fornai F, Bassi L, Torracca MT, Alessandri MG, Scalori V, Corsini GU (1996) Region- and neurotransmitter-dependent species and strain differences in DSP-4-induced monoamine depletion in rodents. Neurodegeneration 5:241-249 (Pubitemid 26360052)
21. Fritschy JM, Grzanna R (1991) Selective effects of DSP-4 on locus coeruleus axons: are there pharmacologically different types of noradrenergic axons in the central nervous system? Prog Brain Res 88:257-268
22. Fritschy JM, Geffard M, Grzanna R (1990) The response of noradrenergic axons to systemically administered DSP-4 in the rat: an immunohistochemical study using antibodies to noradrenaline and dopamine-beta-hydroxylase. J Chem Neuroanat 3:309-321 (Pubitemid 20254159)
23. German DC, Manaye KF, White CL III, Woodward DJ, McIntire DD, Smith WK, Kalaria RN, Mann DM (1992) Disease-specific patterns of locus coeruleus cell loss. Ann Neurol 32:667-676
24. Gesi M, Soldani P, Giorgi FS, Santinami A, Bonaccorsi I, Fornai F (2000) The role of the locus coeruleus in the development of Parkinson's disease. Neurosci Biobehav Rev 24:655-668 (Pubitemid 30625131)
25. Gordon JT, Kaminski DM, Rozanov CB, Dratman MB (1999) Evidence that 3,3′,5-triiodothyronine is concentrated in and delivered from the locus coeruleus to its noradrenergic targets via anterograde axonal transport. Neuroscience 93:943-954 (Pubitemid 29341641)
26. Hallman H, Jonsson G (1984) Pharmacological modifications of the neurotoxic action of the noradrenaline neurotoxin DSP4 on central noradrenaline neurons. Eur J Pharmacol 103:269-278 (Pubitemid 14028983)
27. Hallman H, Sundstrom E, Jonsson G (1984) Effects of the noradrenaline neurotoxin DSP 4 on monoamine neurons and their transmitter turnover in rat CNS. J Neural Transm 60:89-102 (Pubitemid 14035427)
28. Hammond EM, Denko NC, Dorie MJ, Abraham RT, Giaccia AJ (2002) Hypoxia links ATR and p53 through replication arrest. Mol Cell Biol 22:1834-1843 (Pubitemid 34174999)
29. Hatip-Al-Khatib I, Bolukbasi F (1999) Destruction of the noradrenergic system with DSP4 potentiates the behavioral effects of MK-801 in rats. Pharmacol Biochem Behav 62:233-237 (Pubitemid 29070886)
30. Heneka MT, Galea E, Gavriluyk V, Dumitrescu-Ozimek L, Daeschner J, O'Banion MK, Weinberg G, Klockgether T, Feinstein DL (2002) Noradrenergic depletion potentiates beta-amyloid-induced cortical inflammation: implications for Alzheimer's disease. J Neurosci 22:2434-2442 (Pubitemid 37465791)
31. Heneka MT, Ramanathan M, Jacobs AH et al (2006) Locus coeruleus degeneration promotes Alzheimer pathogenesis in amyloid precursor protein 23 transgenic mice. J Neurosci 26:1343-1354 (Pubitemid 43237005)
32. Howard BD, Cho AK, Zhang MB, Koide M, Lin S (1990) Covalent labeling of the cocaine-sensitive catecholamine transporter. J Neurosci Res 26:149-158 (Pubitemid 20197819)
33. Iversen LL (1971) Role of transmitter uptake mechanisms in synaptic neurotransmission. Br J Pharmacol 41:571-591
34. Jaim-Etcheverry G, Zieher LM (1980) DSP-4: a novel compound with neurotoxic effects on noradrenergic neurons of adult and developing rats. Brain Res 188:513-523 (Pubitemid 10144294)
35. Jardanhazi-Kurutz D, Kummer MP, Terwel D, Vogel K, Dyrks T, Thiele A, Heneka MT (2010) Induced LC degeneration in APP/PS1 transgenic mice accelerates early cerebral amyloidosis and cognitive deficits. Neurochem Int 57:375-382
36. Jeppesen DK, Bohr VA, Stevnsner T (2011) DNA repair deficiency in neurodegeneration. Prog Neurobiol 94:166-200
37. Jonsson G, Hallman H, Ponzio F, Ross S (1981) DSP4 (N-(2-chloroethyl)-N- ethyl-2-bromobenzylamine) - a useful denervation tool for central and peripheral noradrenaline neurons. Eur J Pharmacol 72:173-188 (Pubitemid 11072495)
38. Kalinin S, Feinstein DL, Xu HL, Huesa G, Pelligrino DA, Galea E (2006) Degeneration of noradrenergic fibres from the locus coeruleus causes tight-junction disorganisation in the rat brain. Eur J Neurosci 24:3393-3400 (Pubitemid 44952606)
39. Kastan MB, Lim DS (2000) The many substrates and functions of ATM. Nat Rev Mol Cell Biol 1:179-186
40. Katyal S, McKinnon PJ (2008) DNA strand breaks, neurodegeneration and aging in the brain. Mech Ageing Dev 129:483-491
41. Kaufman S, Friedman S (1965) Dopamine-beta-hydroxylase. Pharmacol Rev 17:71-100
42. Kim ST, Lim DS, Canman CE, Kastan MB (1999) Substrate specificities and identification of putative substrates of ATM kinase family members. J Biol Chem 274:37538-37543 (Pubitemid 30026807)
43. Kim CH, Zabetian CP, Cubells JF, Cho S, Biaggioni I, Cohen BM, Robertson D, Kim KS (2002) Mutations in the dopamine beta-hydroxylase gene are associated with human norepinephrine deficiency. Am J Med Genet 108:140-147 (Pubitemid 34174318)
44. Kobayashi K, Morita S, Mizuguchi T, Sawada H, Yamada K, Nagatsu I, Fujita K, Nagatsu T (1994) Functional and high level expression of human dopamine beta-hydroxylase in transgenic mice. J Biol Chem 269:29725-29731 (Pubitemid 24365132)
45. Kurose A, Tanaka T, Huang X, Traganos F, Darzynkiewicz Z (2006) Synchronization in the cell cycle by inhibitors of DNA replication induces histone H2AX phosphorylation: an indication of DNA damage. Cell Prolif 39:231-240
46. Lavin MF (1999) ATM: the product of the gene mutated in ataxia-telangiectasia. Int J Biochem Cell Biol 31:735-740 (Pubitemid 29333116)
47. Lee CM, Javitch JA, Snyder SH (1982) Characterization of [3H]desipramine binding associated with neuronal norepinephrine uptake sites in rat brain membranes. J Neurosci 2:1515-1525 (Pubitemid 13255870)
48. Liu Z, Martin LJ (2001) Motor neurons rapidly accumulate DNA single-strand breaks after in vitro exposure to nitric oxide and peroxynitrite and in vivo axotomy. J Comp Neurol 432:35-60 (Pubitemid 32187019)
49. Liu LF, Desai SD, Li TK, Mao Y, Sun M, Sim SP (2000) Mechanism of action of camptothecin. Ann N Y Acad Sci 922:1-10 (Pubitemid 32050237)
50. Lode HN, Bruchelt G, Seitz G, Gebhardt S, Gekeler V, Niethammer D, Beck J (1995) Reverse transcriptase-polymerase chain reaction (RT-PCR) analysis of monoamine transporters in neuroblastoma cell lines: correlations to meta-iodobenzylguanidine (MIBG) uptake and tyrosine hydroxylase gene expression. Eur J Cancer 31A:586-590
51. Lyons WE, Fritschy JM, Grzanna R (1989) The noradrenergic neurotoxin DSP-4 eliminates the coeruleospinal projection but spares projections of the A5 and A7 groups to the ventral horn of the rat spinal cord. J Neurosci 9:1481-1489 (Pubitemid 19146246)
52. Mann DM, Yates PO, Hawkes J (1982) The noradrenergic system in Alzheimer and multi-infarct dementias. J Neurol Neurosurg Psychiatry 45:113-119 (Pubitemid 12176925)
53. Matsukawa M, Nakadate K, Ishihara I, Okado N (2003) Synaptic loss following depletion of noradrenaline and/or serotonin in the rat visual cortex: a quantitative electron microscopic study. Neuroscience 122:627-635 (Pubitemid 37410284)
54. McGowan CH, Russell P (2004) The DNA damage response: sensing and signaling. Curr Opin Cell Biol 16:629-633 (Pubitemid 39463112)
55. Murren JR, Beidler DR, Cheng YC (1996) Camptothecin resistance related to drug-induced down-regulation of topoisomerase I and to steps occurring after the formation of protein-linked DNA breaks. Ann N Y Acad Sci 803:74-92 (Pubitemid 27057976)
56. Prieto M, Giralt MT (2001) Effects of N-(2-chloroethyl)-N-ethyl-2- bromobenzylamine (DSP4) on alpha2-adrenoceptors which regulate the synthesis and release of noradrenaline in the rat brain. Pharmacol Toxicol 88:152-158
57. Pugh PL, Vidgeon-Hart MP, Ashmeade T et al (2007) Repeated administration of the noradrenergic neurotoxin N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine (DSP-4) modulates neuroinflammation and amyloid plaque load in mice bearing amyloid precursor protein and presenilin-1 mutant transgenes. J Neuroinflammation 4:8 (Pubitemid 46390777)
58. Ransom RW, Waggaman LA, Cho AK (1985) Interaction of xylamine with peripheral sympathetic neurons. Life Sci 37:1177-1182 (Pubitemid 16243141)
59. Rass U, Ahel I, West SC (2007) Defective DNA repair and neurodegenerative disease. Cell 130:991-1004 (Pubitemid 47410275)
60. Rey NL, Jardanhazi-Kurutz D, Terwel D, Kummer MP, Jourdan F, Didier A, Heneka MT (2012) Locus coeruleus degeneration exacerbates olfactory deficits in APP/PS1 transgenic mice. Neurobiol Aging 33:426.e1-426.e11
61. Richards ML, Sadee W (1986) Human neuroblastoma cell lines as models of catechol uptake. Brain Res 384:132-137 (Pubitemid 16001363)
62. Robinson GB, Fluharty SJ, Zigmond MJ, Sclabassi RJ, Berger TW (1993) Recovery of hippocampal dentate granule cell responsiveness to entorhinal cortical input following norepinephrine depletion. Brain Res 614:21-28 (Pubitemid 23181147)
63. Robison SH, Bradley WG (1984) DNA damage and chronic neuronal degenerations. J Neurol Sci 64:11-20 (Pubitemid 14149182)
64. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273:5858-5868 (Pubitemid 28124064)
65. Ross SB (1976) Long-term effects of N-2-chlorethyl-N-ethyl-2- bromobenzylamine hydrochloride on noradrenergic neurones in the rat brain and heart. Br J Pharmacol 58:521-527
66. Rouse J, Jackson SP (2002) Interfaces between the detection, signaling, and repair of DNA damage. Science 297:547-551 (Pubitemid 34815330)
67. Serrano MA, Li Z, Dangeti M, Musich PR, Patrick S, Roginskaya M, Cartwright B, Zou Y (2012) DNA-PK, ATM and ATR collaboratively regulate p53-RPA interaction to facilitate homologous recombination DNA repair. Oncogene 32(19):2452-2462
68. Shiloh Y (2001) ATM and ATR: networking cellular responses to DNA damage. Curr Opin Genet Dev 11:71-77 (Pubitemid 32119281)
69. Shiloh Y (2003) ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer 3:155-168 (Pubitemid 37328868)
70. Sontag TA, Hauser J, Kaunzinger I, Gerlach M, Tucha O, Lange KW (2008) Effects of the noradrenergic neurotoxin DSP4 on spatial memory in the rat. J Neural Transm 115:299-303
71. Srinivasan J, Schmidt WJ (2004) Behavioral and neurochemical effects of noradrenergic depletions with N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine in 6-hydroxydopamine-induced rat model of Parkinson's disease. Behav Brain Res 151:191-199 (Pubitemid 38501442)
72. Szot P, Miguelez C, White SS, Franklin A, Sikkema C, Wilkinson CW, Ugedo L, Raskind MA (2010) A comprehensive analysis of the effect of DSP4 on the locus coeruleus noradrenergic system in the rat. Neuroscience 166:279-291
73. Tieu K, Zuo DM, Yu PH (1999) Differential effects of staurosporine and retinoic acid on the vulnerability of the SH-SY5Y neuroblastoma cells: involvement of bcl-2 and p53 proteins. J Neurosci Res 58:426-435 (Pubitemid 29508576)
74. Ward IM, Chen J (2001) Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J Biol Chem 276:47759-47762
75. Waterman SA, Harding CF (2008) Neurotoxic effects of DSP-4 on the central noradrenergic system in male zebra finches. Behav Brain Res 188:271-280
76. Wenge B, Bonisch H (2009) Interference of the noradrenergic neurotoxin DSP4 with neuronal and nonneuronal monoamine transporters. Naunyn Schmiedebergs Arch Pharmacol 380:523-529
77. Winkler H (1976) The composition of adrenal chromaffin granules: an assessment of controversial results. Neuroscience 1:65-80
78. Wolfman C, Abo V, Calvo D, Medina J, Dajas F, Silveira R (1994) Recovery of central noradrenergic neurons one year after the administration of the neurotoxin DSP4. Neurochem Int 25:395-400 (Pubitemid 24295014)
79. Yu PH, Davis BA, Fang J, Boulton AA (1994) Neuroprotective effects of some monoamine oxidase-B inhibitors against DSP-4-induced noradrenaline depletion in the mouse hippocampus. J Neurochem 63:1820-1828 (Pubitemid 24326226)
80. Zarei M, Stephenson JD (2002) Effects of DSP4 and dizolcipine on connectivity of solid E19 cortical grafts to ablated SmI region of adult rats; an in vivo electrophysiological study. Brain Res 947:182-190
81. Zarow C, Lyness SA, Mortimer JA, Chui HC (2003) Neuronal loss is greater in the locus coeruleus than nucleus basalis and substantia nigra in Alzheimer and Parkinson diseases. Arch Neurol 60:337-341 (Pubitemid 36314358)
82. Zhang J, Perry G, Smith MA, Robertson D, Olson SJ, Graham DG, Montine TJ (1999) Parkinson's disease is associated with oxidative damage to cytoplasmic DNA and RNA in substantia nigra neurons. Am J Pathol 154:1423-1429 (Pubitemid 29226437)
83. Zhou BB, Elledge SJ (2000) The DNA damage response: putting checkpoints in perspective. Nature 408:433-439
84. Zigmond RE, Schwarzschild MA, Rittenhouse AR (1989) Acute regulation of tyrosine hydroxylase by nerve activity and by neurotransmitters via phosphorylation. Annu Rev Neurosci 12:415-461 (Pubitemid 19085457)
85. Zou Y, Liu Y, Wu X, Shell SM (2006) Functions of human replication protein A (RPA): from DNA replication to DNA damage and stress responses. J Cell Physiol 208:267-273 (Pubitemid 43993416)