Amphetamine and environmentally induced hyperthermia differentially alter the expression of genes regulating vascular tone and angiogenesis in the meninges and associated vasculature

Synapse

Volumn 63, Issue 10, 2009, Pages 881-894

  Thomas, Monzy ^a   George, Nysia I ^a   Patterson, Tucker A ^a   Bowyer, John F ^a,b  

^a NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

^b NCTR   (United States)

Author keywords

Amphetamines; Blood brain barrier; Gene expression; Meninges; Vasculature

Indexed keywords

AMPHETAMINE; CONNECTIVE TISSUE GROWTH FACTOR; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GELATINASE A; HEAT SHOCK PROTEIN 72; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN; PROTEIN KINASE B; RNA; SODIUM CHLORIDE; SOMATOMEDIN; SOMATOMEDIN B; SOMATOMEDIN C; TISSUE INHIBITOR OF METALLOPROTEINASE 1; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARACHNOID; ARTICLE; BLOOD VESSEL TONE; BRAIN REGION; CONTROLLED STUDY; CORPUS STRIATUM; CYTOKINE RELEASE; ENVIRONMENTAL FACTOR; FOREBRAIN; GENE EXPRESSION REGULATION; HEAT SHOCK; HEAT STRESS; HOMEOSTASIS; HYPERTHERMIA; INFLAMMATION; MALE; MENINX; NONHUMAN; NUCLEOTIDE SEQUENCE; PARIETAL LOBE; PIA MATER; PRIORITY JOURNAL; PROTEIN ISOLATION; RAT; SPRAGUE DAWLEY RAT; VASCULARIZATION; VASODILATATION;

AMPHETAMINE; ANIMALS; BLOOD VESSELS; BODY TEMPERATURE; BRAIN; CENTRAL NERVOUS SYSTEM STIMULANTS; CONNECTIVE TISSUE GROWTH FACTOR; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENVIRONMENT; FEVER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HSP72 HEAT-SHOCK PROTEINS; MALE; MENINGES; NEOVASCULARIZATION, PHYSIOLOGIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS; VASOACTIVE INTESTINAL PEPTIDE;

EID: 70349100464     PISSN: 08874476     EISSN: 10982396     Source Type: Journal    
DOI: 10.1002/syn.20661     Document Type: Article

References (75)

1. Amenta F, Ricci A, Vega JA. 1991. Autoradiographic localization of dopamine receptors in rat cerebral blood vessels. Eur J Pharmacol 192:123-132.
2. Benarroch EE. 2007. Neurovascular unit dysfunction: A vascular component of Alzheimer disease? Neurology 68:1730-1732.
3. Boulton M, Flessner M, Armstrong D, Mohamed R, Hay J, Johnston M. 1999. Contribution of extracranial lymphatics and arachnoid villi to the clearance of a CSF tracer in the rat. Am J Physiol 276(3 Part 2):R818-R823. (Pubitemid 29157512)
4. Bowyer JF, Ali S. 2006. High doses of methamphetamine that cause disruption of the blood-brain barrier in limbic regions produce extensive neuronal degeneration in mouse hippocampus. Synapse 60:521-532. (Pubitemid 44537085)
5. Bowyer JF, Holson RR. 1995. Methamphetamine and amphetamine neurotoxicity: Characteristics, interactions with body temperature and possible mechanisms. In: Chang LW, Dyer RS, editors. Handbook of neurotoxicology. New York: Marcel Dekker Inc. p 845-870.
6. Bowyer JF, Schmued LC. 2006. Fluoro-Ruby labeling prior to an amphetamine neurotoxic insult shows a definitive massive loss of dopaminergic terminals and axons in the caudate-putamen. Brain Res 1075:236-239.
7. Bowyer JF, Davies DL, Schmued L, Broening HW, Newport GD, Slikker W Jr, Holson RR. 1994. Further studies of the role of hyperthermia in methamphetamine neurotoxicity. J Pharmacol Exp Ther 268:1571-1580. (Pubitemid 24100380)
8. Bowyer JF, Peterson SL, Rountree RL, Tor-Agbidye J, Wang GJ. 1998. Neuronal degeneration in rat forebrain resulting from D-amphetamine-induced convulsions is dependent on seizure severity and age. Brain Res 809:77-90. (Pubitemid 29003428)
9. Bowyer JF, Harris AJ, Delongchamp RR, Jakab RL, Miller DB, Little AR, O'Callaghan JP. 2004. Selective changes in gene expression in cortical regions sensitive to amphetamine during the neurodegenerative process. Neurotoxicology 25:555-572.
10. Bowyer JF, Pogge AR, Delongchamp RR, O'Callaghan JP, Patel KM, Vrana KE, Freeman WM. 2007. A threshold neurotoxic amphetamine exposure inhibits parietal cortex expression of synaptic plasticity-related genes. Neuroscience 144:66-76.
11. Bowyer JF, Robinson B, Ali S, Schmued LC. 2008a. Neurotoxic-related changes in tyrosine hydroxylase, microglia, myelin, and the blood-brain barrier in the caudate-putamen from acute methamphetamine exposure. Synapse 62:193-204. (Pubitemid 351186400)
12. Bowyer JF, Thomas MT, Schmued LC, Ali SF. 2008b. Brain region-specific neurodegenerative profiles showing the relative importance of amphetamine dose, hyperthermia, seizures and the blood-brain barrier. Ann N Y Acad Sci 1139:127-139.
13. Bradbury MW. 1984. The structure and function of the blood-brain barrier. Fed Proc 43:186-190.
14. Burnstock G. 1985. Neurogenic control of cerebral circulation. Cephalalgia 5(Suppl 2):25-33.
15. Choi JK, Chen YI, Hamel E, Jenkins BG. 2006. Brain hemodynamic changes mediated by dopamine receptors: Role of the cerebral microvasculature in dopamine-mediated neurovascular coupling. Neuroimage 30:700-712.
16. Chomczynski P, Mackey K. 1995. Short technical reports. Modification of the TRI reagent procedure for isolation of RNA from polysaccharide- and proteoglycan-rich sources. Biotechniques 19:942-945.
17. Cines DB, Pollak ES, Buck CA, Loscalzo J, Zimmerman GA, McEver RP, Pober JS, Wick TM, Konkle BA, Schwartz BS, Barnathan ES, McCrae KR, Hug BA, Schmidt AM, Stern DM. 1998. Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood 91:3527-3561. (Pubitemid 28225719)
18. Commins DL, Seiden LS. 1986. α-Methyltyrosine blocks methylamphetamine-induced degeneration in the rat somatosensory cortex. Brain Res 365:15-20.
19. Cross MJ, Claesson-Welsh L. 2001. FGF and VEGF function in angiogenesis: Signalling pathways, biological responses and therapeutic inhibition. Trends Pharmacol Sci 22:201-207. (Pubitemid 32244307)
20. Dahlqvist K, Umemoto EY, Brokaw JJ, Dupuis M, McDonald DM. 1999. Tissue macrophages associated with angiogenesis in chronic airway inflammation in rats. Am J Respir Cell Mol Biol 20:237-247. (Pubitemid 129504883)
21. Deng X, Wang Y, Chou J, Cadet JL. 2001. Methamphetamine causes widespread apoptosis in the mouse brain: Evidence from using an improved TUNEL histochemical method. Brain Res Mol Brain Res 93:64-69. (Pubitemid 32786903)
22. Dono R, Texido G, Dussel R, Ehmke H, Zeller R. 1998. Impaired cerebral cortex development and blood pressure regulation in FGF-2-deficient mice. EMBO J 17:4213-4225. (Pubitemid 28362612)
23. Dumont DJ, Fong GH, Puri MC, Gradwohl G, Alitalo K, Breitman ML. 1995. Vascularization of the mouse embryo: a study of flk-1, tek, tie, and vascular endothelial growth factor expression during development. Dev Dyn 203:80-92.
24. Eisch AJ, Schmued LC, Marshall JF. 1998. Characterizing cortical neuron injury with Fluoro-Jade labeling after a neurotoxic regimen of methamphetamine. Synapse 30:329-333.
25. Fagan SC, Hess DC, Hohnadel EJ, Pollock DM, Ergul A. 2004. Targets for vascular protection after acute ischemic stroke. Stroke 35:2220-2225. (Pubitemid 39129589)
26. Faraci FM. 1989. Effects of endothelin and vasopressin on cerebral blood vessels. Am J Physiol 257(3 Part 2):H799-H803.
27. Franklin SS. 2005. Arterial stiffness and hypertension: A two-way street? Hypertension 45:349-351.
28. Franklin TB, Krueger-Naug AM, Clarke DB, Arrigo AP, Currie RW. 2005. The role of heat shock proteins Hsp70 and Hsp27 in cellular protection of the central nervous system. Int J Hyperthermia 21:379-392.
29. Hamel E. 2006. Perivascular nerves and the regulation of cerebrovascular tone. J Appl Physiol 100:1059-1064. (Pubitemid 43671565)
30. Hess A, Desiderio C, McAuliffe WG. 1990. Acute neuropathological changes in the caudate nucleus caused by MPTP and methamphetamine: Immunohistochemical studies. J Neurocytol 19:338-342. (Pubitemid 20222709)
31. Hynynen MM, Khalil RA. 2006. The vascular endothelin system in hypertension - Recent patents and discoveries. Recent Pat Cardiovasc Drug Discov 1:95-108.
32. Iadecola C. 2004. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat Rev Neurosci 5:347-360. (Pubitemid 38568496)
33. Innes IR, Nickerson M. 1975. Norepinephrine, epinephrine, and sympathomimetic amines. In: Goodman LS, Gilman A, editors. The pharmacological basis of therapeutics, 5th ed. New York, NY: MacMillan Publishing Co. p 477-513.
34. Inoki I, Shiomi T, Hashimoto G, Enomoto H, Nakamura H, Makino K, Ikeda E, Takata S, Kobayashi K, Okada Y. 2002. Connective tissue growth factor binds vascular endothelial growth factor (VEGF) and inhibits VEGF-induced angiogenesis. FASEB J 16:219-221.
35. Jakab RL, Bowyer JF. 2002. Parvalbumin neuron circuits and microglia in three dopamine-poor cortical regions remain sensitive to amphetamine exposure in the absence of hyperthermia, seizure and stroke. Brain Res 958:52-69.
36. Johanson CE, Duncan JA III, Klinge PM, Brinker T, Stopa EG, Silverberg GD. 2008. Multiplicity of cerebrospinal fluid functions: New challenges in health and disease. Cerebrospinal Fluid Res 5:10. (Pubitemid 351803829)
37. Johnston M, Zakharov A, Koh L, Armstrong D. 2005. Subarachnoid injection of microfil reveals connections between cerebrospinal fluid and nasal lymphatics in the non-human primate. Neuropathol Appl Neurobiol 31:632-640. (Pubitemid 41668373)
38. Kalant H, Kalant OJ. 1975. Death in amphetamine users: Causes and rates. Can Med Assoc J 112:299-304.
39. Kitazono T, Heistad DD, Faraci FM. 1995. Dilatation of the basilar artery in response to selective activation of endothelin B receptors in vivo. J Pharmacol Exp Ther 273:1-6.
40. Krimer LS, Muly EC III, Williams GV, Goldman-Rakic PS. 1998. Dopaminergic regulation of cerebral cortical microcirculation. Nat Neurosci 1:286-289. (Pubitemid 128652674)
41. Kulik T, Kusano Y, Aronhime S, Sandler AL, Winn HR. 2008. Regulation of cerebral vasculature in normal and ischemic brain. Neuropharmacology 55:281-288.
42. Lavallee M, Takamura M, Parent R, Thorin E. 2001. Crosstalk between endothelin and nitric oxide in the control of vascular tone. Heart Fail Rev 6:265-276. (Pubitemid 32725185)
43. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408. (Pubitemid 34164012)
44. Logan A, Gonzalez AM, Hill DJ, Berry M, Gregson NA, Baird A. 1994. Coordinated pattern of expression and localization of insulin-like growth factor-II (IGF-II) and IGF-binding protein-2 in the adult rat brain. Endocrinology 135:2255-2264. (Pubitemid 24363926)
45. McGee SM, McGee DN, McGee MB. 2004. Spontaneous intracerebral hemorrhage related to methamphetamine abuse: Autopsy findings and clinical correlation. Am J Forensic Med Pathol 25:334-337.
46. Miller MA, Coon TP. 2006. Re: Delayed ischemic stroke associated with methamphetamine use. J Emerg Med 31:305-306; author reply 306.
47. Mulligan SJ, MacVicar BA. 2004. Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 431:195-199.
48. O'Callaghan JP, Miller DB. 2001. Neurotoxic effects of substituted amphetamines in rats and mice. In: Massaro EJ, editor. Handbook of neurotoxicology. Totowa, NJ: Humana Press Inc. p 269-301.
49. Pasqualini R, Koivunen E, Kain R, Lahdenranta J, Sakamoto M, Stryhn A, Ashmun RA, Shapiro LH, Arap W, Ruoslahti E. 2000. Aminopeptidase N is a receptor for tumor-homing peptides and a target for inhibiting angiogenesis. Cancer Res 60:722-727. (Pubitemid 30094573)
50. Pepper MS. 1997. Manipulating angiogenesis. From basic science to the bedside. Arterioscler Thromb Vasc Biol 17:605-619.
51. Pozzi M, Roccatagliata D, Sterzi R. 2008. Drug abuse and intracranial hemorrhage. Neurol Sci 29(Suppl 2):S269-S270.
52. Reed MJ, Koike T, Sadoun E, Sage EH, Puolakkainen P. 2003. Inhibition of TIMP1 enhances angiogenesis in vivo and cell migration in vitro. Microvasc Res 65:9-17. (Pubitemid 36263285)
53. Ricaurte GA, McCann UD. 2005. Recognition and management of complications of new recreational drug use. Lancet 365:2137-2145.
54. Rothrock JF, Rubenstein R, Lyden PD. 1988. Ischemic stroke associated with methamphetamine inhalation. Neurology 38:589-592. (Pubitemid 18105294)
55. Schmued LC, Bowyer JF. 1997. Methamphetamine exposure can produce neuronal degeneration in mouse hippocampal remnants. Brain Res 759:135-140.
56. Seiden LS, Sabol KE. 1995. Neurotoxicity of methamphetamine-related drugs and cocaine. In: Chang LW, Dyer RS, editors. Handbook of neurotoxicology. New York, Basel, Hong Kong: Marcel Dekker, Inc. p 824-844.
57. Seiden LS, Fischman MW, Schuster CR. 1976. Long-term methamphetamine induced changes in brain catecholamines in tolerant rhesus monkeys. Drug Alcohol Depend 1:215-219.
58. Sharma HS, Sjoquist PO, Ali SF. 2007. Drugs of abuse-induced hyperthermia, blood-brain barrier dysfunction and neurotoxicity: Neuroprotective effects of a new antioxidant compound H-290/51. Curr Pharm Des 13:1903-1923.
59. Shim JS, Kim JH, Cho HY, Yum YN, Kim SH, Park HJ, Shim BS, Choi SH, Kwon HJ. 2003. Irreversible inhibition of CD13/aminopeptidase N by the antiangiogenic agent curcumin. Chem Biol 10:695-704.
60. Sriram K, Miller DB, O'Callaghan JP. 2006. Minocycline attenuates microglial activation but fails to mitigate striatal dopaminergic neurotoxicity: Role of tumor necrosis factor-α. J Neurochem 96:706-718.
61. Tata DA, Yamamoto BK. 2007. Interactions between methamphetamine and environmental stress: Role of oxidative stress, glutamate and mitochondrial dysfunction. Addiction 102(Suppl 1):49-60.
62. Thomas DM, Dowgiert J, Geddes TJ, Francescutti-Verbeem D, Liu X, Kuhn DM. 2004a. Microglial activation is a pharmacologically specific marker for the neurotoxic amphetamines. Neurosci Lett 367:349-354. (Pubitemid 39178611)
63. Thomas DM, Francescutti-Verbeem DM, Liu X, Kuhn DM. 2004b. Identification of differentially regulated transcripts in mouse striatum following methamphetamine treatment - An oligonucleotide microarray approach. J Neurochem 88:380-393. (Pubitemid 38084554)
64. Thomas DM, Walker PD, Benjamins JA, Geddes TJ, Kuhn DM. 2004c. Methamphetamine neurotoxicity in dopamine nerve endings of the striatum is associated with microglial activation. J Pharmacol Exp Ther 311:1-7.
65. Thomas M, Harrell JM, Morishima Y, Peng HM, Pratt WB, Lieberman AP. 2006. Pharmacologic and genetic inhibition of hsp90-dependent trafficking reduces aggregation and promotes degradation of the expanded glutamine androgen receptor without stress protein induction. Hun Mol Genet 15:1876-1883. (Pubitemid 43821778)
66. Thomas M, Yu Z, Dadgar N, Varambally S, Yu J, Chinnaiyan AM, Lieberman AP. 2005. The unfolded protein response modulates toxicity of the expanded glutamine androgen receptor. J Biol Chem 280:21264-21271. (Pubitemid 40805689)
67. Tuncel N, Erkasap N, Sahinturk V. 2000. The effect of stress and in vivo vasoactive intestinal peptide (VIP) treatment on the response of isolated rat aorta to norepinephrine, angiotensin II and vasopressin, and adventitial mast cells. Stress 3:299-308. (Pubitemid 32294349)
68. Turkmen S, Dogan S, Barutcu I, Sipahi I, Ayabakan H, Esen AM, Esen O, Guzelsoy D. 2005. The changes in circulating levels of vasoactive intestinal polypeptide during exercise and its reproducibility for detection of myocardial ischemia. Int Heart J 46:363-371.
69. Walter HJ, Berry M, Hill DJ, Cwyfan-Hughes S, Holly JM, Logan A. 1999. Distinct sites of insulin-like growth factor (IGF)-II expression and localization in lesioned rat brain: Possible roles of IGF binding proteins (IGFBPs) in the mediation of IGF-II activity. Endocrinology 140:520-532. (Pubitemid 29011199)
70. Wang Y, Hayashi T, Chang CF, Chiang YH, Tsao LI, Su TP, Borlongan C, Lin SZ. 2001. Methamphetamine potentiates ischemia/reperfusion insults after transient middle cerebral artery ligation. Stroke 32:775-782. (Pubitemid 32208734)
71. Wei GZ, Zhang J, Sheng SL, Ai HX, Ma JC, Lui HB. 1993. Increased plasma endothelin-1 concentration in patients with acute cerebral infarction and actions of endothelin-1 on pial arterioles of rat. Chin Med J (Engl) 106:917-921.
72. Winslow BT, Voorhees KI, Pehl KA. 2007. Methamphetamine abuse. Am Fam Physician 76:1169-1174.
73. Wolf K, Tsakiris DA, Weber R, Erb P, Battegay M. 2002. Antiretroviral therapy reduces markers of endothelial and coagulation activation in patients infected with human immunodeficiency virus type 1. J Infect Dis 185:456-462. (Pubitemid 34142807)
74. Yuan J, Hatzidimitriou G, Suthar P, Mueller M, McCann U, Ricaurte G. 2006. Relationship between temperature, dopaminergic neurotoxicity, and plasma drug concentrations in methamphetamine-treated squirrel monkeys. J Pharmacol Exp Ther 316:1210-1218. (Pubitemid 43345296)
75. Zhang ZG, Chopp M, Zaloga C, Pollock JS, Forstermann U. 1993. Cerebral endothelial nitric oxide synthase expression after focal cerebral ischemia in rats. Stroke 24:2016-2021; discussion 2021-2022. (Pubitemid 23352737)