Cocaine exposure in vitro induces apoptosis in fetal locus coeruleus neurons through TNF-α-mediated induction of Bax and phosphorylated c-Jun NH2-terminal kinase

Journal of Neurochemistry

Volumn 103, Issue 2, 2007, Pages 542-556

  Dey, Swatee ^a,b   Snow, Diane M ^b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Apoptosis; Cocaine; Drug abuse; Noradrenergic; Rat; Tumor necrosis factor

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; CASPASE 3; COCAINE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN BAX; RECOMBINANT TUMOR NECROSIS FACTOR ALPHA; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN NERVE CELL; CELL ASSAY; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; FEMALE; IN VITRO STUDY; LOCUS CERULEUS; METABOLIC ACTIVATION; NERVE CELL NECROSIS; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; CASPASE 3; CELL SURVIVAL; CELLS, CULTURED; COCAINE; CULTURE MEDIA; CYCLIN D1; DATA INTERPRETATION, STATISTICAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; IN SITU NICK-END LABELING; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LOCUS COERULEUS; NEURONS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PREGNANCY; RATS; RATS, LONG-EVANS; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TETRAZOLIUM SALTS; THIAZOLES; TUMOR NECROSIS FACTOR-ALPHA;

RATTUS;

EID: 34848870042     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.04750.x     Document Type: Article

References (70)

1. Ashkenazi A. Dixit V. M. (1998) Death receptors: signaling and modulation. Science 281, 1305 1308.
2. Bae S. Zhang L. (2005) Prenatal cocaine exposure increases apoptosis of neonatal rat heart and heart susceptibility to ischemia-reperfusion injury in 1-month-old rat. Br. J. Pharmacol. 144, 900 907.
3. Barker V., Middleton G., Davey F. Davies A. M. (2001) TNFalpha contributes to the death of NGF-dependent neurons during development. Nat. Neurosci. 4, 1194 1198.
4. Baselt R. C. (1983) Stability of cocaine in biological fluids. J. Chromatogr. 268, 502 505.
5. Bayer S. A., Altman J., Russo R. J. Zhang X. (1993) Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 14, 83 144.
6. Bouis P., Taccard G. Boelsterli U. A (1990) Determination of cocaine and norcocaine in plasma and cell cultures using high-performance liquid chromatography. J. Chromatogr. 526, 447 459.
7. Bouret S. Sara S. J. (2004) Reward expectation, orientation of attention and locus coeruleus-medial frontal cortex interplay during learning. Eur. J. Neurosci. 20, 791 802.
8. Breder C. D., Tsujimoto M., Terano Y., Scott D. W. Saper C. B. (1993) Distribution and characterization of tumor necrosis factor-alpha-like immunoreactivity in the murine central nervous system. J. Comp. Neurol. 337, 543 567.
9. Bunney E. B., Appel S. B. Brodie M. S. (2000) Cocaine potentiates ethanol-induced excitation of dopaminergic reward neurons in the ventral tegmental area. J. Pharmacol. Exp. Ther. 293, 383 389.
10. Burgunder J. M. Young III. W. S. (1990) Ontogeny of tyrosine hydroxylase and cholecystokinin gene expression in the rat mesencephalon. Brain Res. Dev. Brain Res. 52, 85 93.
11. Chang H. Y. Yang X. (2000) Proteases for cell suicide: functions and regulation of caspases. Microbiol. Mol. Biol. Rev. 64, 821 846.
12. Darnay B. G. Aggarwal B. B. (1997) Early events in TNF signaling: a story of associations and dissociations. J. Leukoc. Biol. 61, 559 566.
13. Dey S., Mactutus C. F., Booze R. M. Snow D. M. (2006) Specificity of prenatal cocaine on inhibition of locus coeruleus neurite outgrowth. Neuroscience 139, 899 907.
14. Dey S., Mactutus C. F., Booze R. M. Snow D. M. (2007) Cocaine exposure in vitro induces apoptosis in fetal locus coeruleus neurons by altering the Bax/Bcl-2 ratio and through caspase-3 apoptotic signaling. Neuroscience 144, 509 521.
15. Evans S. M., Cone E. J. Henningfield J. E. (1996) Arterial and venous cocaine plasma concentrations in humans: relationship to route of administration, cardiovascular effects and subjective effects. J. Pharmacol. Exp. Ther. 279, 1345 1356.
16. Fiala M., Gan X. H., Zhang L. et al. (1998) Cocaine enhances monocyte migration across the blood-brain barrier. Cocaine's connection to AIDS dementia and vasculitis? Adv. Exp. Med. Biol. 437, 199 205.
17. Foltz T. L., Snow D. M., Strupp B. J., Booze R. M. Mactutus C. F. (2004) Prenatal intravenous cocaine and the heart rate-orienting response: a dose-response study. Int. J. Dev. Neurosci. 22, 285 296.
18. Gan X., Zhang L., Berger O. et al. (1999) Cocaine enhances brain endothelial adhesion molecules and leukocyte migration. Clin. Immunol. 91, 68 76.
19. Green D. R. (1998) Apoptotic pathways: the roads to ruin. Cell 94, 695 698.
20. Grell M., Zimmermann G., Gottfried E. et al. (1999) Induction of cell death by tumour necrosis factor (TNF) receptor 2, CD40 and CD30: a role for TNF-R1 activation by endogenous membrane-anchored TNF. EMBO J. 18, 3034 3043.
21. Gupta S. Gollapudi S. (2005) Molecular mechanisms of TNF-alpha-induced apoptosis in aging human T cell subsets. Int. J. Biochem. Cell Biol. 37, 1034 1042.
22. Haeberlein S. L. (2004) Mitochondrial function in apoptotic neuronal cell death. Neurochem. Res. 29, 521 530.
23. He J., Xiao Y. Zhang L (2000a) Cocaine induces apoptosis in human coronary artery endothelial cells. J. Cardiovasc. Pharmacol. 35, 572 580.
24. He J., Xiao Y., Casiano C. A. Zhang L (2000b) Role of mitochondrial cytochrome c in cocaine-induced apoptosis in coronary artery endothelial cells. J. Pharmacol. Exp. Ther. 295, 896 903.
25. Heffelfinger A. K., Craft S., White D. A. Shyken J. (2002) Visual attention in preschool children prenatally exposed to cocaine: implications for behavioral regulation. J. Int. Neuropsychol. Soc. 8, 12 21.
26. Ignatowski T. A. Spengler R. N. (1994) Tumor necrosis factor-alpha: presynaptic sensitivity is modified after antidepressant drug administration. Brain Res. 665, 293 299.
27. Ignatowski T. A., Chou R. C. Spengler R. N. (1996) Changes in noradrenergic sensitivity to tumor necrosis factor-alpha in brains of rats administered clonidine. J. Neuroimmunol. 70, 55 63.
28. Ignatowski T. A., Noble B. K., Wright J. R., Gorfien J. L., Heffner R. R. Spengler R. N. (1997) Neuronal-associated tumor necrosis factor (TNF alpha): its role in noradrenergic functioning and modification of its expression following antidepressant drug administration. J. Neuroimmunol. 79, 84 90.
29. Isenschmid D. S., Levine B. S. Caplan Y. H. (1989) A comprehensive study of the stability of cocaine and its metabolites. J. Anal. Toxicol. 13, 250 256.
30. Johnson G. L. Lapadat R (2002) Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 298, 1911 1912.
31. Jones L. B., Stanwood G. D., Reinoso B. S., Washington R. A., Wang H. Y., Friedman E. Levitt P (2000) In utero cocaine-induced dysfunction of dopamine D1 receptor signaling and abnormal differentiation of cerebral cortical neurons. J. Neurosci. 20, 4606 4614.
32. Kinouchi K., Brown G., Pasternak G. Donner D. B. (1991) Identification and characterization of receptors for tumor necrosis factor-alpha in the brain. Biochem. Biophys. Res. Commun. 181, 1532 1538.
33. Koistinaho M. Koistinaho J. (2002) Role of p38 and p44/42 mitogen-activated protein kinases in microglia. Glia 40, 175 183.
34. Konig N., Wilkie M. B. Lauder J. (1989) Dissection of monoaminergic neuronal groups from embryonic rat brain, in A Dissection and Tissue Culture Manual of the Nervous System (Sahar A., Vellis J. D., Vernadakis A. Haber B., eds), pp. 26 29. Alan R. Liss Inc., New York.
35. Lauder J. M. Bloom F. E. (1974) Ontogeny of monoamine neurons in the locus coeruleus, Raphe nuclei and substantia nigra of the rat. I. Cell differentiation. J. Comp. Neurol. 155, 469 481.
36. Lee Y. W., Hennig B., Fiala M., Kim K. S. Toborek M. (2001) Cocaine activates redox-regulated transcription factors and induces TNF-alpha expression in human brain endothelial cells. Brain Res. 920, 125 133.
37. Li G., Xiao Y. Zhang L (2005a) Cocaine induces apoptosis in fetal rat myocardial cells through the p38 mitogen-activated protein kinase and mitochondrial/cytochrome c pathways. J. Pharmacol. Exp. Ther. 312, 112 119.
38. Li Y. P., Chen Y., John J., Moylan J., Jin B., Mann D. L. Reid M. B. (2005b) TNF-alpha acts via p38 MAPK to stimulate expression of the ubiquitin ligase atrogin1/MAFbx in skeletal muscle. FASEB J. 19, 362 370.
39. Lidow M. S. Song Z. M. (2001) Primates exposed to cocaine in utero display reduced density and number of cerebral cortical neurons. J. Comp. Neurol. 435, 263 275.
40. Mactutus C. F. (1999) Prenatal intravenous cocaine adversely affects attentional processing in preweanling rats. Neurotoxicol. Teratol. 21, 539 550.
41. Meldrum D. R. (1998) Tumor necrosis factor in the heart. Am. J. Physiol. 274, R577 R595.
42. Mogi M., Harada M., Riederer P., Narabayashi H., Fujita K. Nagatsu T (1994) Tumor necrosis factor-alpha (TNF-alpha) increases both in the brain and in the cerebrospinal fluid from parkinsonian patients. Neurosci. Lett. 165, 208 210.
43. Muller N (1997) Role of the cytokine network in the CNS and psychiatric disorders. Nervenarzt 68, 11 20.
44. Nakada S., Kawano T., Saito-akita S., Iwase S., Horiguchi-Yamada J., Ohno T. Yamada H (2001) MEK and p38MAPK inhibitors potentiate TNF-alpha induced apoptosis in U937 cells. Anticancer Res. 21, 167 171.
45. Nassogne M. C., Evrard P. Courtoy P. J. (1995) Selective neuronal toxicity of cocaine in embryonic mouse brain cocultures. Proc. Natl Acad. Sci. USA 92, 11029 11033.
46. Nassogne M. C., Louahed J., Evrard P. Courtoy P. J. (1997) Cocaine induces apoptosis in cortical neurons of fetal mice. J. Neurochem. 68, 2442 2450.
47. Nassogne M. C., Evrard P. Courtoy P. J. (1998) Selective direct toxicity of cocaine on fetal mouse neurons. Teratogenic implications of neurite and apoptotic neuronal loss. Ann. NY Acad. Sci. 846, 51 68.
48. Nicholson D. W., Ali A., Thornberry N. A. et al. (1995) Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376, 37 43.
49. Noland J. S., Singer L. T., Short E. J., Minnes S., Arendt R. E., Kirchner H. L. Bearer C. (2005) Prenatal drug exposure and selective attention in preschoolers. Neurotoxicol. Teratol. 27, 429 438.
50. Novikova S. I., He F., Bai J. Lidow M. S. (2005a) Neuropathology of the cerebral cortex observed in a range of animal models of prenatal cocaine exposure may reflect alterations in genes involved in the Wnt and cadherin systems. Synapse 56, 105 116.
51. Novikova S. I., He F., Bai J., Badan I., Lidow I. A. Lidow M. S. (2005b) Cocaine-induced changes in the expression of apoptosis-related genes in the fetal mouse cerebral wall. Neurotoxicol. Teratol. 27, 3 14.
52. Oliver F. J., de la Rubia G., Rolli V., Ruiz-Ruiz M. C., de Murcia G. Murcia J. M. (1998) Importance of poly(ADP-ribose) polymerase and its cleavage in apoptosis. Lesson from an uncleavable mutant. J. Biol. Chem. 273, 33533 33539.
53. Park J. G., Yuk Y., Rhim H., Yi S. Y. Yoo Y. S. (2002) Role of p38 MAPK in the regulation of apoptosis signaling induced by TNF-alpha in differentiated PC12 cells. J. Biochem. Mol. Biol. 35, 267 272.
54. Richardson G. A., Conroy M. L. Day N. L. (1996) Prenatal cocaine exposure: effects on the development of school-age children. Neurotoxicol. Teratol. 18, 627 634.
55. Snow D. M., Smith J. D., Booze R. M., Welch M. A. Mactutus C. F. (2001) Cocaine decreases cell survival and inhibits neurite extension of rat locus coeruleus neurons. Neurotoxicol. Teratol. 23, 225 234.
56. Snow D. M., Carman H. M., Smith J. D., Booze R. M., Welch M. Mactutus C. F. (2004) Cocaine-induced inhibition of process outgrowth in locus coeruleus neurons: role of gestational exposure period and offspring sex. Int. J. Dev. Neurosci. 22, 297 308.
57. Stanwood G. D., Washington R. A. Levitt P (2001) Identification of a sensitive period of prenatal cocaine exposure that alters the development of the anterior cingulate cortex. Cereb. Cortex 11, 430 440.
58. Takao T., Tracey D. E., Mitchell W. M. De Souza E. B. (1990) Interleukin-1 receptors in mouse brain: characterization and neuronal localization. Endocrinology 127, 3070 3078.
59. Tezel G., Yang X., Yang J. Wax M. B. (2004) Role of tumor necrosis factor receptor-1 in the death of retinal ganglion cells following optic nerve crush injury in mice. Brain Res. 996, 202 212.
60. Tournier C., Hess P., Yang D. D., Xu J., Turner T. K., Nimnual A., Bar-Sagi D., Jones S. N., Flavell R. A. Davis R. J. (2000) Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 288, 870 874.
61. Tsuruta F., Sunayama J., Mori Y., Hattori S., Shimizu S., Tsujimoto Y., Yoshioka K., Masuyama N. Gotoh Y (2004) JNK promotes Bax translocation to mitochondria through phosphorylation of 14-3-3 proteins. EMBO J. 23, 1889 1899.
62. Vorhees C. V., Reed T. M., Acuff-Smith K. D., Schilling M. A., Cappon G. D., Fisher J. E. Pu C. (1995) Long-term learning deficits and changes in unlearned behaviors following in utero exposure to multiple daily doses of cocaine during different exposure periods and maternal plasma cocaine concentrations. Neurotoxicol. Teratol. 17, 253 264.
63. Wada T. Penninger J. M. (2004) Mitogen-activated protein kinases in apoptosis regulation. Oncogene 23, 2838 2849.
64. Wang J. F., Ren X., DeAngelis J., Min J., Zhang Y., Hampton T. G., Amende I. Morgan J. P. (2001) Differential patterns of cocaine-induced organ toxicity in murine heart versus liver. Exp. Biol. Med. (Maywood) 226, 52 60.
65. Wang J. F., Yang Y., Sullivan M. F., Min J., Cai J., Zeldin D. C., Xiao Y. F. Morgan J. P. (2002) Induction of cardiac cytochrome p450 in cocaine-treated mice. Exp. Biol. Med. (Maywood) 227, 182 188.
66. Wu K. L., Chan S. H., Chao Y. M. Chan J. Y. (2003) Expression of pro-inflammatory cytokine and caspase genes promotes neuronal apoptosis in pontine reticular formation after spinal cord transection. Neurobiol. Dis. 14, 19 31.
67. Xiao Y., Xiao D., He J. Zhang L (2001) Maternal cocaine administration during pregnancy induces apoptosis in fetal rat heart. J. Cardiovasc. Pharmacol. 37, 639 648.
68. Yanase N., Hata K., Shimo K., Hayashida M., Evers B. M. Mizuguchi J (2005) Requirement of c-Jun NH2-terminal kinase activation in interferon-alpha-induced apoptosis through upregulation of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) in Daudi B lymphoma cells. Exp. Cell Res. 310, 10 21.
69. Zhang L., Xiao Y. He J (1999) Cocaine and apoptosis in myocardial cells. Anat. Rec. 257, 208 216.
70. Zhu J., Liu M., Kennedy R. H. Liu S. J. (2006) TNF-alpha-induced impairment of mitochondrial integrity and apoptosis mediated by caspase-8 in adult ventricular myocytes. Cytokine 34, 96 105.