Effect of Temperature on Dopamine Transporter Function and Intracellular Accumulation of Methamphetamine: Implications for Methamphetamine-induced Dopaminergic Neurotoxicity

Overview

Journal J Neurosci

Specialty Neurology

Date 2000 Oct 12

PMID 11027249

Citations 37

Authors

T Xie

U D McCann

S Kim

J Yuan

G A Ricaurte

Affiliations

Soon will be listed here.

Abstract

Hyperthermia exacerbates and hypothermia attenuates methamphetamine (METH)-induced dopamine (DA) neurotoxicity. The mechanisms underlying these temperature effects are unknown. Given the essential role of the DA transporter (DAT) in the expression of METH-induced DA neurotoxicity, we hypothesized that the effect of temperature on METH-induced DA neurotoxicity is mediated, at least in part, at the level of the DAT. To test this hypothesis, the effects of small, physiologically relevant temperature changes on DAT function were evaluated in two types of cultured neuronal cells: (1) a neuroblastoma cell line stably transfected with human DAT cDNA and (2) rat embryonic mesencephalic primary cells that naturally express the DAT. Temperatures for studies of DAT function were selected based on core temperature measurements in animals exposed to METH under usual ambient (22 degrees C) and hypothermic (6 degrees C) temperature conditions, where METH neurotoxicity was fully expressed and blocked, respectively. DAT function, determined by measuring accumulation of radiolabeled DA and 1-methyl-4-phenylpyridinium (MPP(+)), was found to directly correlate with temperature, with higher levels of substrate uptake at 40 degrees C, intermediate levels at 37 degrees C, and lower levels at 34 degrees C. DAT-mediated accumulation of METH also directly correlated with temperature, with greater accumulation at higher temperatures. These findings indicate that relatively small, physiologically relevant changes in temperature significantly alter DAT function and intracellular METH accumulation, and suggest that the effect of temperature on METH-induced DA neurotoxicity is mediated, at least in part, at the level of the DAT.

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References

Sonsalla P, Riordan D, Heikkila R . Competitive and noncompetitive antagonists at N-methyl-D-aspartate receptors protect against methamphetamine-induced dopaminergic damage in mice. J Pharmacol Exp Ther. 1991; 256(2):506-12. View

Ricaurte G, Langston J, DELANNEY L, Irwin I, Brooks J . Dopamine uptake blockers protect against the dopamine depleting effect of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) in the mouse striatum. Neurosci Lett. 1985; 59(3):259-64. DOI: 10.1016/0304-3940(85)90141-7. View

Callahan B, Ricaurte G . Effect of 7-nitroindazole on body temperature and methamphetamine-induced dopamine toxicity. Neuroreport. 1998; 9(12):2691-5. DOI: 10.1097/00001756-199808240-00001. View

Cubells J, Rayport S, Rajendran G, Sulzer D . Methamphetamine neurotoxicity involves vacuolation of endocytic organelles and dopamine-dependent intracellular oxidative stress. J Neurosci. 1994; 14(4):2260-71. PMC: 6577123. View

Malberg J, Seiden L . Small changes in ambient temperature cause large changes in 3,4-methylenedioxymethamphetamine (MDMA)-induced serotonin neurotoxicity and core body temperature in the rat. J Neurosci. 1998; 18(13):5086-94. PMC: 6792575. View

Pifl C, Giros B, Caron M . Dopamine transporter expression confers cytotoxicity to low doses of the parkinsonism-inducing neurotoxin 1-methyl-4-phenylpyridinium. J Neurosci. 1993; 13(10):4246-53. PMC: 6576397. View

Miller D, OCallaghan J . Environment-, drug- and stress-induced alterations in body temperature affect the neurotoxicity of substituted amphetamines in the C57BL/6J mouse. J Pharmacol Exp Ther. 1994; 270(2):752-60. View

Burrows K, Nixdorf W, Yamamoto B . Central administration of methamphetamine synergizes with metabolic inhibition to deplete striatal monoamines. J Pharmacol Exp Ther. 2000; 292(3):853-60. View

Pu C, Fisher J, Cappon G, Vorhees C . The effects of amfonelic acid, a dopamine uptake inhibitor, on methamphetamine-induced dopaminergic terminal degeneration and astrocytic response in rat striatum. Brain Res. 1994; 649(1-2):217-24. DOI: 10.1016/0006-8993(94)91067-7. View

10.

Fumagalli F, Gainetdinov R, Valenzano K, Caron M . Role of dopamine transporter in methamphetamine-induced neurotoxicity: evidence from mice lacking the transporter. J Neurosci. 1998; 18(13):4861-9. PMC: 6792558. View

11.

Gainetdinov R, Fumagalli F, Jones S, Caron M . Dopamine transporter is required for in vivo MPTP neurotoxicity: evidence from mice lacking the transporter. J Neurochem. 1997; 69(3):1322-5. DOI: 10.1046/j.1471-4159.1997.69031322.x. View

12.

Woolverton W, Ricaurte G, FORNO L, Seiden L . Long-term effects of chronic methamphetamine administration in rhesus monkeys. Brain Res. 1989; 486(1):73-8. DOI: 10.1016/0006-8993(89)91279-1. View

13.

Broening H, Bowyer J, Slikker Jr W . Age-dependent sensitivity of rats to the long-term effects of the serotonergic neurotoxicant (+/-)-3,4-methylenedioxymethamphetamine (MDMA) correlates with the magnitude of the MDMA-induced thermal response. J Pharmacol Exp Ther. 1995; 275(1):325-33. View

14.

Koob G, Bloom F . Cellular and molecular mechanisms of drug dependence. Science. 1988; 242(4879):715-23. DOI: 10.1126/science.2903550. View

15.

Zaczek R, Culp S, Goldberg H, McCann D, DE SOUZA E . Interactions of [3H]amphetamine with rat brain synaptosomes. I. Saturable sequestration. J Pharmacol Exp Ther. 1991; 257(2):820-9. View

16.

Bowyer J, Clausing P, Schmued L, Davies D, Binienda Z, Newport G . Parenterally administered 3-nitropropionic acid and amphetamine can combine to produce damage to terminals and cell bodies in the striatum. Brain Res. 1996; 712(2):221-9. DOI: 10.1016/0006-8993(95)01417-9. View

17.

Javitch J, DAmato R, Strittmatter S, Snyder S . Parkinsonism-inducing neurotoxin, N-methyl-4-phenyl-1,2,3,6 -tetrahydropyridine: uptake of the metabolite N-methyl-4-phenylpyridine by dopamine neurons explains selective toxicity. Proc Natl Acad Sci U S A. 1985; 82(7):2173-7. PMC: 397515. DOI: 10.1073/pnas.82.7.2173. View

18.

Sonsalla P, Jochnowitz N, Zeevalk G, Oostveen J, Hall E . Treatment of mice with methamphetamine produces cell loss in the substantia nigra. Brain Res. 1996; 738(1):172-5. DOI: 10.1016/0006-8993(96)00995-x. View

19.

Donovan D, Miner L, Perry M, Revay R, SHARPE L, Przedborski S . Cocaine reward and MPTP toxicity: alteration by regional variant dopamine transporter overexpression. Brain Res Mol Brain Res. 1999; 73(1-2):37-49. DOI: 10.1016/s0169-328x(99)00235-1. View

20.

Moy L, Albers D, Sonsalla P . Lowering ambient or core body temperature elevates striatal MPP+ levels and enhances toxicity to dopamine neurons in MPTP-treated mice. Brain Res. 1998; 790(1-2):264-9. DOI: 10.1016/s0006-8993(98)00069-9. View