Acute effects of pulsed microwaves and 3-nitropropionic acid on neuronal ultrastructure in the rat caudate-putamen

Bioelectromagnetics

Volumn 26, Issue 2, 2005, Pages 82-101

  Seaman, Ronald L ^a   Phelix, Clyde F ^b  

^a USAF   (United States)

^b UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

Author keywords

Chemical hypoxia; Endoplasmic reticulum; Mitochondria; Nuclear envelope; Stereology; Striatum

Indexed keywords

CELL MEMBRANES; MICROSTRUCTURE; MITOCHONDRIA; PULSE REPETITION RATE; RATS;

3-NITROPROPIONIC ACIDS; CHEMICAL HYPOXIA; ENDOPLASMIC RETICULUM; MICROWAVE EXPOSURE; MITOCHONDRIAS; NUCLEAR ENVELOPE; PULSED MICROWAVES; SPECIFIC ABSORPTION RATE; STEREOLOGY; STRIATUM;

NEURONS;

3 NITROPROPIONIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY SYSTEM; CAUDATE NUCLEUS; CELL DENSITY; CELL METABOLISM; CELL NUCLEUS MEMBRANE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; DOSIMETRY; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM; MALE; MICROWAVE RADIATION; MOTOR ACTIVITY; NERVE CELL; NERVE CELL LESION; NONHUMAN; PRIORITY JOURNAL; PUTAMEN; RADIATION ABSORPTION; RAT; RAT STRAIN;

ANIMALIA; MUS;

EID: 12844253203     PISSN: 01978462     EISSN: None     Source Type: Journal    
DOI: 10.1002/bem.20054     Document Type: Article

References (130)

1. Albert EN, DeSantis M. 1975. Do microwaves alter nervous system structure? Ann NY Acad Sci 247:87-106.
2. Albert EN, Sherif M. 1988. Morphological changes in cerebellum of neonatal rats exposed to 2.45 GHz microwaves. Prog Clin Biol Res 257:135-151.
3. Albin RL. 2000. Basal ganglia neurotoxins. Neurol Clin 18:665-680.
4. Alexi T, Hughes PE, Knusel B, Tobin AJ. 1998a. Metabolic compromise with systemic 3-nitropropionic acid produces striatal apoptosis in Sprague-Dawley rats but not in BALB/c ByJ mice. Exp Neurol 153:74-93.
5. Alexi T, Hughes PE, Faull RLM, Williams CE. 1998b. 3-nitropropionic acid's lethal triplet: Cooperative pathways of neurodegeneration. Neuroreport 9:R57-R64.
6. Antonawich FJ, Fiore-Marasa SM, Parker CP. 2002. Modulation of apoptotic regulatory proteins and early activation of cytochrome C following systemic 3-nitropropionic acid administration. Brain Res Bull 57:647-649.
7. Arber SL, Neilly JP, Lin JC, Kriho V. 1986. The effect of 2450 MHz microwave radiation on the ultrastructure of snail neurons. Physiol Chem Phys Med NMR 18:243-249.
8. Baranski S. 1972. Histological and histochemical effect of microwave irradiation on the central nervous system of rabbits and guinea pigs. Am J Phys Med 51:182-191.
9. Beal MF. 1992. Does impairment of energy metabolism result in excitotoxic neuronal death in neurodegenerative illnesses? Ann Neurol 31:119-130.
10. Beal MF, Brouillet E, Jenkins BG, Ferrante RJ, Kowall NW, Miller JM, Storey E, Srivastava R, Rosen BR, Hyman BT. 1993a. Neurochemical and histologic characterization of striatal excitotoxic lesions produced by the mitochondrial toxin 3-nitropropionic acid. J Neurosci 13:4181-4192.
11. Beal MF, Brouillet E, Jenkins B, Henshaw R, Rosen B, Hyman BT. 1993b. Age-dependent striatal excitotoxic lesions produced by the endogenous mitochondrial inhibitor malonate. J Neurochem 61:1147-1150.
12. Beal MF, Ferrante RJ, Henshaw R, Matthews RT, Chan PH, Kowall NW, Epstein CJ, Schulz JB. 1995. 3-nitropropionic acid neurotoxicity is attenuated in copper/zinc superoxide dismutase transgenic mice. J Neurochem 65:919-922.
13. Binienda Z, Kim CS. 1997. Increase in levels of total free fatty acids in rat brain regions following 3-nitropropionic acid administration. Neurosci Lett 230:199-201.
14. Bizat N, Hermel JM, Boyer F, Jacquard C, Créminion C, Ouary S, Escartin C, Hantraye P, Krajewski S, Brouillet E. 2003. Calpain is a major cell death effector in selective striatal degeneration induced in vivo by 3-nitropropionate: Implications for Huntington's disease. J Neurosci 23:5020-5030.
15. Blum D, Galas MC, Gall D, Cuvelier L, Schiffmann SN. 2002. Striatal and cortical neurochemical changes induced by chronic metabolic compromise in the 3-nitropropionic model of Huntington's disease. Neurobiol Dis 10:410-426.
16. Blum D, Galas MC, Cuvelier L, Schiffmann SN. 2004. Chronic intoxication with 3-nitropropionic acid in rats induces the loss of striatal dopamine terminals without affecting nigral cell viability. Neurosci Lett 354:234-238.
17. Boehning D, Patterson RL, Sedaghat L, Glebova NO, Kurosaki T, Snyder SH. 2003. Cytochrome c binds to inositol (1,4,5) triphosphate receptors, amplifying calcium-dependent apoptosis. Nat Cell Biol 5:1051-1060.
18. Borlongan CV, Koutouzis TK, Freeman TB, Cahill DW, Sanberg PR. 1995a. Behavioral pathology induced by repeated systemic injections of 3-nitropropionic acid mimics the motoric symptoms of Huntington's disease. Brain Res 697:254-257.
19. Borlongan CV, Koutouzis TK, Randall TS, Freeman TB, Cahill DW, Sanberg PR. 1995b. Systemic 3-nitropropionic acid: Behavioral deficits and striatal damage in adult rats. Brain Res Bull 36:549-556.
20. Brambrink AM, Schneider A, Noga H, Astheimer A, Götz B, Körner I, Heimann A, Welschof M, Kempski O. 2000. Tolerance-inducing dose of 3-nitropropionic acid modulates bcl-2 and bax balance in the rat brain: A potential mechanism of chemical preconditioning. J Cereb Blood Flow Metab 20:1425-1436.
21. Breckenridge DG, Germain M, Mathai JP, Nguyen M, Shore GC. 2003. Regulation of apoptosis by endoplasmic reticulum pathways. Oncogene 22:8608-8618.
22. Brouillet E, Jenkins BG, Hyman BT, Ferrante RJ, Kowall NW, Srivastava R, Roy DS, Rosen BR, Beal MF. 1993. Age-dependent vulnerability of the striatum to the mitochondrial toxin 3-nitropropionic acid. J Neurochem 60:356-359.
23. Brouillet E, Hantraye P, Ferrante RJ, Dolan R, Leroy-Willig A, Kowall NW, Beal MF. 1995. Chronic mitochondrial energy impairment produces selective striatal degeneration and abnormal choreiform movements in primates. Proc Natl Acad Sci USA 92:7105-7109.
24. Brouillet E, Guyot MC, Mittoux V, Altairac S, Condé F, Palfi S, Hantraye P. 1998. Partial inhibition of brain succinate dehydrogenase by 3-nitropropionic acid is sufficient to initiate striatal degeneration in rat. J Neurochem 70:794-805.
25. Brouillet E, Condé F, Beal MF, Hantraye P. 1999. Replicating Huntington's disease phenotype in experimental animals. Prog Neurobiol 59:427-468.
26. Budd SL. 1998. Mechanisms of neuronal damage in brain hypoxia/ischemia: Focus on the role of mitochondrial calcium accumulation. Pharmacol Ther 80:203-229.
27. Calabresi P, Centonze D, Pisani A, Sancesario G, Gubellini P, Marfia GA, Bernardi G. 1998. Striatal spiny neurons and cholinergic interneurons express differential ionotropic glutamatergic responses and vulnerability: Implication for ischemia and Huntington's disease. Ann Neurol 43:586-597.
28. Calabresi P, Centonze D, Gubellini P, Marfia GA, Pisani A, Sancesario G, Bernardi G. 2000. Synaptic transmission in the striatum: From plasticity to neurodegeneration. Prog Neurobiol 61:231-265.
29. Cepeda C, Walsh JP, Hull CD, Howard SG, Buchwald NA, Levine MS. 1989. Dye-coupling in the neostriatum of the rat: I. Modulation by dopamine-depleting lesions. Synapse 4:229-237.
30. Chang HT, Kitai ST. 1982. Large neostriatal neurons in the rat: An electron microscopic study of gold-toned Golgi-stained cells. Brain Res Bull 8:631-643.
31. Chou CK, Guy AW, McDougall JA, Lai H. 1985. Specific absorption rate in rats exposed to 2450 MHz microwaves under seven exposure conditions. Bioelectromagnetics 6:73-88.
32. 2-weighted, diffusion-weighted, and perfusion magnetic resonance imaging. Neuroscience 92:1035-1041.
33. Cotrina JL, Lin JHC, Alves-Rodrigues A, Liu S, Li J, Azmi-Ghadimi H, Kang J, Naus CCG, Nedergaard M. 1998. Connexins regulate calcium signaling by controlling ATP release. Proc Natl Acad Sci USA 95:15735-15740.
34. D'Andrea JA, de Lorge JO. 1990. Behavioral effects of electromagnetic fields. In: Gandhi OP, editor. Biological effects and medical applications of electromagnetic energy. Englewood Cliffs, NJ: Prentice Hall. pp 319-338.
35. Dautry C, Vaufrey F, Brouillet E, Bizat N, Henry PG, Condé F, Bloch G, Hantraye P. 2000. Early N-acetylaspartate depletion is a marker of neuronal dysfunction in rats and primates chronically treated with the mitochondrial toxin 3-nitropropionic acid. J Cereb Blood Flow Metab 20:789-799.
36. Deeter DP, Gaydos JC, editors. 1993. Occupational health: The soldier and the industrial base. Washington DC: Office of the Surgeon General, US Department of the Army. 643p.
37. DeFrank JJ, Bryan PK, Hicks CW, Jr., Sliney DH. 1993. Ch. 15, Nonionizing radiation. In: Textbook of military medicine, Part III, Vol. 2. Washington DC: Office of the Surgeon General, US Department of the Army. pp 539-580.
38. Duan W, Guo Z, Mattson MP. 2000. Participation of Par-4 in the degeneration of striatal neurons induced by metabolic compromise with 3-nitropropionic acid. Exp Neurol 165:1-11.
39. Durney CH, Massoudi H, Iskander MF. 1986. Radiofrequency radiation dosimetry handbook, 4th edn.Technical Report USAFSAM-TR-85-73. Brooks Air Force Base: USAF School of Aerospace Medicine.
40. Eldridge J, editor. 2001. Jane's nuclear, biological and chemical defence. Alexandria, Virginia: Jane's Information Group, Inc. 386p.
41. Foster KR, Schwan HP. 1986. Dielectric properties of tissues. In: Polk C, Postow E, editors. CRC handbook of biological effects of electromagnetic fields. Boca Raton: CRC Press. pp 27-96.
42. Fritze K, Wiessner C, Kuster N, Sommer C, Gass P, Hermann DM, Kiessling M, Hossmann KA. 1997. Effect of global system for mobile communication microwave exposure on the genomic response of the rat brain. Neuroscience 81:627-639.
43. 2+ overload induced by a mitochondrial toxin, 3-nitropropionic acid. Neuroscience 87:497-507.
44. Galas MC, Bizat N, Cuvelier L, Bantubungi K, Brouillet E, Schiffmann SN, Blum D. 2004. Death of cortical and striatal neurons induced by mitochondrial defect involves differential molecular mechanisms. Neurobiol Dis 15:152-159.
45. Garcia M, Vanhoutte P, Pages C, Besson MJ, Brouillet E, Caboche J. 2002. The mitochondrial toxin 3-nitropropionic acid induces striatal neurodegeneration via a c-Jun N-terminal kinase/c-Jun module. J Neurosci 22:2174-2184.
46. Gordon CJ, Long MD, Fehlner KS, Stead AG. 1986. Body temperature in the mouse, hamster, and rat exposed to radiofrequency radiation: An interspecies comparison. J Therm Biol 11:59-65.
47. Gould DH, Gustine DL. 1982. Basal ganglia degeneration, myelin alterations, and enzyme inhibition induced in mice by the plant toxin 3-nitropropanoic acid. Neuropathol Appl Neurobiol 8:377-393.
48. Gould DH, Wilson MP, Hamar DW. 1985. Brain enzyme and clinical alterations induced in rats and mice by nitroaliphatic toxicants. Toxicol Lett 27:83-89.
49. Gundersen HJG, Bendtsen TF, Korbo L, Marcussen N, Møller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sørensen FB, Vesterby A, West MJ. 1988. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 96:379-394.
50. Guy AW, Wallace J, McDougall JA. 1979. Circularly polarized 2450-MHz waveguide system for chronic exposure of small animals to microwaves. Radiol Sci 14:63-74.
51. Guyot MC, Hantraye P, Dolan R, Palfi S, Maziére M, Brouillet E. 1997. Quantifiable bradykinesia, gait abnormalities and Huntington's disease-like striatal lesions in rats chronically treated with 3-nitropropionic acid. Neuroscience 79:45-56.
52. Haley RW, Fleckenstein JL, Marshall WW, McDonald GG, Kramer GL, Petty F. 2000. Effect of basal ganglia injury on central dopamine activity in Gulf War syndrome. Arch Neurol 57:1280-1285.
53. Hamilton BF, Gould DH. 1987. Nature and distribution of brain lesions in rats intoxicated with 3-nitropropionic acid: A type of hypoxic (energy deficient) brain damage. Acta Neuropathol (Berl) 72:286-297.
54. Hansson HA. 1988. Effects on the nervous system by exposure to electromagnetic fields: Experimental and clinical studies. Prog Clin Biol Res 257:119-134.
55. Hansson E, Rönnbäck L. 2003. Glial neuronal signaling in the central nervous system. FASEB J 17:341-348.
56. Heales SJR, Bolaños JP, Stewart VC, Brookes PS, Land JM, Clark JB. 1999. Nitric oxide, mitochondria and neurological disease. Biochim Biophys Acta 1410:215-228.
57. Joellenbeck LM, Russell PK, Guze SB, editors. 1999. Strategies to protect the health of deployed US forces: Medical surveillance, record keeping, and risk reduction. Washington DC: National Academy Press. 282p.
58. Kalimo H, Garcia JH, Kamijyo Y, Tanaka J, Trump BF. 1977. The ultrastructure of "brain death". I. Electron microscopy of feline cerebral cortex after complete ischemia. Virchows Arch B Cell Pathol 25:207-220.
59. Kalimo H, Auer RN, Siesjö BK. 1985. The temporal evolution of hypoglycemic brain damage. III. Light- and electron-microscopic findings in the rat caudoputamen. Acta Neuropathol (Berl) 67:37-50.
60. Kalns J, Ryan KL, Mason PA, Bruno JG, Gooden R, Kiel JL. 2000. Oxidative stress precedes circulatory failure induced by 35-GHz microwave heating. Shock 13:52-59.
61. Kawaguchi Y. 1997. Neostriatal cell subtypes and their functional roles. Neurosci Res 27:1-8.
62. Keene CD, Rodrigues CMP, Eich T, Linehan-Stieers C, Abt A, Kren BT, Steer CJ, Low WC. 2001. A bile acid protects against motor and cognitive deficits and reduces striatal degeneration in the 3-nitropropionic acid model of Huntington's disease. Exp Neurol 171:351-360.
63. Kita H, Kitai ST. 1988. Glutamate decarboxylase immunoreactive neurons in rat neostriatum: Their morphological types and populations. Brain Res 447:346-352.
64. Kodsi MH, Swerdlow NR. 1997. Mitochondrial toxin 3-nitropropionic acid produces startle reflex abnormalities and striatal damage in rats that model some features of Huntington's disease. Neurosci Lett 231:103-107.
65. La Fontaine MA, Geddes JW, Banks A, Butterfield DA. 2000. 3-nitropropionic acid induced in vivo protein oxidation in striatal and cortical synaptosomes: Insights into Huntington's disease. Brain Res 858:356-362.
66. Lai H. 1994. Neurological effects of radiofrequency electromagnetic radiation. In: Lin JC, editor. Advances in electromagnetic fields in living systems, Vol. 1. New York: Plenum. pp 27-80.
67. Le Feuvre R, Brough D, Rothwell N. 2002. Extracellular ATP and P2X7 receptors in neurodegeneration. Eur J Pharmacol 447:261-269.
68. Lee WT, Lee CS, Pan YL, Chang C. 2000. Temporal changes of cerebral metabolites and striatal lesions in acute 3-nitropropionic acid intoxication in the rat. Mag Res Med 44:29-34.
69. Lee WT, Yin HS, Shen YZ. 2002. The mechanisms of neuronal death produced by mitochondrial toxin 3-nitropropionic acid: The roles of N-methyl-D-aspartate glutamate receptors and mitochondrial calcium overload. Neuroscience 112:707-716.
70. Leszczynski D, Joenvaara S, Reivinen J, Kuokka R. 2002. Non-thermal activation of the hsp27/p38MAPK stress pathway by mobile phone radiation in human endothelial cells: Molecular mechanism for cancer- and blood-brain barrier-related effects. Differentiation 70:120-129.
71. Lin TY, Wang SM, Fu WM, Chen YH, Yin HS. 1999. Toxicity of tunicamycin to cultured brain neurons: Ultrastructure of the degenerating neurons. J Cell Biochem 74:638-647.
72. Lotz WG, Michaelson SM. 1978. Temperature and corticosterone relationships in microwave-exposed rats. J Appl Physiol 44:438-445.
73. Ludolph AC, He F, Spencer PS, Hammerstad J, Sabri M. 1991. 3-Nitropropionic acid - Exogenous animal neurotoxin and possible human striatal toxin. Can J Neurol Sci 18:492-498.
74. Mandile P, Giuditta A, Romano F, Montagnese P, Piscopo S, Cotugno M, Vescia S. 2003. Waking EEG power spectra in the rat: Correlations with training performance. Cogn Brain Res 17:94-105.
75. Martin LJ, Brambrink AM, Price AC, Kaiser A, Agnew DM, Ichord RN, Traystman RJ. 2000. Neuronal death in newborn striatum after hypoxia-ischemia is necrosis and evolves with oxidative stress. Neurobiol Dis 7:169-191.
76. Matthews RT, Yang L, Jenkins BG, Ferrante RJ, Rosen BR, Kaddurah-Daouk R, Beal MF. 1998. Neuroprotective effects of creatine and cyclocreatine in animal models of Huntington's disease. J Neurosci 18:156-163.
77. McIntosh TK, Saatman KE, Raghupathi R, Graham DI, Smith DH, Lee VM, Trojanowski JQ. 1998. The molecular and cellular sequelae of experimental traumatic brain injury: Pathogenetic mechanisms. Neuropathol Appl Neurobiol 24:251-267.
78. Michaelson SM. 1986. Interaction of nonmodulated radio frequency fields with living matter: Experimental results. In: Polk C, Postow E, editors. CRC handbook of biological effects of electromagnetic fields. Boca Raton: CRC Press. pp 339-423.
79. Mitchell IJ, Cooper AJ, Griffiths MR. 1999. The selective vulnerabilibty of striatopallidal neurons. ProgNeurobiol 59:691-719.
80. 2+ increase and cell damage in cultured rat cerebral endothelial cells. Brain Res 956:116-125.
81. NAS (National Academy of Science, Committee to review the health consequences of service during the Persian Gulf War). 1996. Ch. 3, Environment and exposures. In: Health consequences of service during the Persian Gulf War: Recommendations For research and information systems. Washington DC: National Academy Press. pp 36-66.
82. 2+, ATP, mitochondrial membrane potential, and calpain activity on the mechanism of neuron death induced by 3-nitropropionic acid. Neurochem Int 43:89-99.
83. Nishino H, Shimano Y, Kumazaki M, Sakurai T. 1995. Chronically administered 3-nitropropionic acid induces striatal lesions attributed to dysfunction of the blood-brain barrier. Neurosci Lett 186:161-164.
84. Nishino H, Kumazaki M, Fukuda A, Fujimoto I, Shimano Y, Hida H, Sakurai T, Deshpande SB, Shimizu H, Morikawa S, Inubushi T. 1997. Acute 3-nitropropionic acid intoxication induces striatal astrocytic cell death and dysfunction of the blood-brain barrier: Involvement of dopamine toxicity. Neurosci Res 27:343-355.
85. Nony PA, Scallet AC, Rountree RL, Ye X, Binienda Z. 1999. 3-nitropropionic acid (3-NPA) produces hypothermia and inhibits histochemical labeling of succinate dehydrogenase (SDH) in rat brain. Metab Brain Dis 14:83-94.
86. Onn SP, Grace AA. 1994. Dye coupling between rat striatal neurons recorded in vivo: Compartmental organization and modulation by dopamine. J Neurophysiol 71:1917-1934.
87. Onn SP, Grace AA. 1999. Alterations in electrophysiological activity and dye coupling of striatal spiny and aspiny neurons in dopamine-denervated rat striatum recorded in vivo. Synapse 33:1-15.
88. Ouary S, Bizat N, Altairac S, Ménétrat H, Mittoux V, Condé F, Hantraye P, Brouillet E. 2000. Major strain differences in response to chronic systemic administration of the mitochondrial toxin 3-nitropropionic acid in rats: Implications for neuroprotection studies. Neuroscience 97:521-530.
89. Parpura V, Haydon PG. 2000. Physiological astrocytic calcium levels stimulate glutamate release to modulate adjacent neurons. Proc Natl Acad Sci USA 97:8629-8634.
90. Parpura V, Basarsky TA, Liu F, Jeftinija K, Jeftinija S, Haydon PG. 1994. Glutamate-mediated astrocyte-neuron signaling. Nature 369:744-747.
91. Paschen W, Doutheil J. 1999. Disturbances of the functioning of endoplasmic reticulum: A key mechanism underlying neuronal cell injury? J Cereb Blood Flow Metab 19:1-18.
92. Paschen W, Frandsen A. 2001. Endoplasmic reticulum dysfunction - A common denominator for cell injury in acute and degenerative diseases of the brain? J Neurochem 79:719-725.
93. Paskevich PA, Evans HK, Domesick VB. 1991. Morphological assessment of neuronal aggregates in the striatum of the rat. J Comp Neurol 305:361-369.
94. Paxinos G, Watson C. 1986. The rat brain in stereotaxic coordinates, 2nd edn. San Diego: Academic Press.
95. Petito CK, Pulsinelli WA. 1984. Sequential development of reversible and irreversible neuronal damage following cerebral ischemia. J Neuropathol Exp Neurol 43:141-153.
96. Phelan AM, Lange DG, Kues HA, Lutty GA. 1992. Modification of membrane fluidity in melanin-containing cells by low-level microwave radiation. Bioelectromagnetics 13:131-146.
97. Philippova TM, Novoselov VI, Alekseev SI. 1994. Influence of microwaves on different types of receptors and the role of peroxidation of lipids on receptor-protein shedding. Bioelectromagnetics 15:183-192.
98. Pickel VM, Chan J. 1991. Plasmalemmal appositions between cholinergic and non-cholinergic neurons in rat caudateputamen nuclei. Neuroscience 41:459-472.
99. Pollack AE. 2001. Anatomy, physiology, and pharmacology of the basal ganglia. Neurol Clin 19:523-534.
100. Pubill D, Verdaguer E, Canudas AM, Sureda FX, Escubedo E, Camaras J, Pallas M, Camins A. 2001. Orphenadrine prevents 3-nitropropionic acid-induced neurotoxicity in vitro and in vivo. Br J Pharmacol 132:693-702.
101. Russ JC, Dehoff RT. 2001. Practical Stereology, 2nd edn. New York: Plenum Press. 382p.
102. Ryu JK, Kim J, Choi SH, Oh YJ, Lee YB, Kim SU, Jin BK. 2002. ATP-induced in vivo neurotoxicity in the rat striatum via P2 receptors. Neuroreport 13:1611-1615.
103. Ryu JK, Nagai A, Kim J, Lee MC, McLarnon JG, Kim SU. 2003. Microglial activation and cell death induced by the mitochondrial toxin 3-nitropropionic acid: In vitro and in vivo studies. Neurobiol Dis 12:121-132.
104. Salford LG, Brun A, Sturesson K, Eberhardt JL, Persson BR. 1994. Permeability of the blood-brain barrier induced by 915 MHz electromagnetic radiation, continuous wave and modulated at 8, 16, 50, and 200 Hz. Microsc Res Tech 27:535-542.
105. Salford LG, Brun AE, Eberhardt JL, Malmgren L, Persson BRR. 2003. Nerve cell damage in mammalian brain after exposure to microwaves from GSM mobile phones. Environ Health Perspect 111:881-883.
106. Sanders AP, Joines WT. 1984. The effects of hyperthermia and hyperthermia plus microwaves on rat brain energy metabolism. Bioelectromagnetics 5:63-70.
107. Sanders AP, Joines WT, Allis JW. 1985. Effects of continuous-wave, pulsed, and sinusoidal-amplitude-modulated microwaves on brain energy metabolism. Bioelectromagnetics 6:89-97.
108. Schmechel DE. 1999. Assessment of ultrastructural changes associated with apoptosis. In: Hannun YA, Boustany RM, editors. Apoptosis in neurobiology. Boca Raton FL: CRC Press. pp 153-181.
109. Schulz JB, Matthews RT, Jenkin BG, Ferrante RJ, Siwek D, Henshaw DR, Cipolloni PB, Mecocci P, Kowall NW, Rosen BR, Beal MF. 1995. Blockade of neuronal nitric oxide synthase protects against excitotoxicity in vivo. J Neurosci 15:8419-8429.
110. Schulz JB, Henshaw DR, MacGarvey U, Beal MF. 1996. Involvement of oxidative stress in 3-nitropropionic acid neurotoxicity. Neurochem Int 29:167-171.
111. Seaman RL. 2000. Effects of acute systemic 3-nitropropionic acid administration on rat activity and acoustic startle. Neurosci Lett 280:183-186.
112. Seaman RL, Mathur SP, Dick EJ, Jr. 2004. Effects of pulsed microwaves and 3-nitropropionic acid on rat motor activity, acoustic startle, and brain histology. WRAIR/USAMRD Technical Report.
113. Sharma HS, Westman J, Nyberg F. 1998. Pathophysiology of brain edema and cell changes following hyperthermic brain injury. Prog Brain Res 115:351-412.
114. Sidell FR, Takafuji ET, Franz DR, editors. 1997. Medical aspects of chemical and biological warfare. Washington DC: Office of the Surgeon General, US Department of the Army. 721p.
115. Singh N, Rudra N, Bansal P, Mathur R, Behari J, Nayar U. 1994. Poly ADP ribosylation as a possible mechanism of microwave-biointeraction. Indian J Physiol Pharmacol 38:181-184.
116. Söderfeldt B, Kalimo H, Olsson Y, Siesjö BK. 1981. Pathogenesis of brain lesions caused by experimental epilepsy. Light- and electron-microscopic changes in the rat cerebral cortex following bicuculline-induced status epilepticus. Acta Neuropathol (Berl) 54:219-231.
117. Somosy Z. 2000. Radiation response of cell organelles. Micron 31:165-181.
118. Stout CE, Costantin JL, Naus CCG, Charles AC. 2002. Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J Biol Chem 277:10482-10488.
119. Streetly M, editor. 2001. Jane's radar and electronic warfare systems. Alexandria, Virginia: Jane's Information Group, Inc. 651p.
120. Sugino T, Nozaki K, Tokime T, Hashimoto N, Kikuchi H. 1997. 3-nitropropionic acid induces poly(ADP-ribosyl)ation and apoptosis related gene expression in the striatum in vivo. Neurosci Lett 237:121-124.
121. Tolgskaya MS, Gordon ZV. 1973. Pathological effects of radio waves. New York: Consultants Bureau. 146p.
122. Trump BF, Berezesky IK. 1998. The reactions of cells to lethal injury: Oncosis and necrosis - The role of calcium. In: Lockshin RA, Zakeri Z, Tilly JL, editors. When cells die. New York: Wiley-Liss. pp 57-96.
123. 1H nuclear magnetic resonance spectroscopy and biochemical characterization. Neuroscience 79:819-826.
124. Vécsei L, Dibó G, Kiss C. 1998. Neurotoxins and neurodegenerative disorders. Neurotoxicology 19:511-514.
125. Verkhratsky A, Petersen OH. 2002. The endoplasmic reticulum as an integrating signaling organelle: From neuronal signaling to neuronal death. Eur J Pharmacol 447:141-154.
126. Vis JC, Verbeek MM, de Waal RMW, ten Donkelaar HJ, Kremer HPH. 1999. 3-Nitropropionic acid induces a spectrum of Huntington's disease-like neuropathology in rat striatum. Neuropathol Appl Neurobiol 25:513-521.
127. Vorobyov VV, Schibaev NV, Morelli M, Carta AR. 2003. EEG modifications in the cortex and striatum after dopaminergic priming in the 6-hydroxydopamine rat model of Parkinson's disease. Brain Res 972:177-185.
128. Wiegand F, Liao W, Busch C, Castell S, Knapp F, Lindauer U, Megow D, Meisel A, Redetzky A, Ruscher K, Trendelenburg G, Victorov I, Riepe M, Diener HC, Dirnagl U. 1999. Respiratory chain inhibition induces tolerance to focal cerebral ischemia. J Cereb Blood Flow Metab 19:1229-1237.
129. Williamson J, editor. 1997. Jane's military communications. Alexandria, Virginia: Jane's Information Group, Inc. 845p.
130. Wüllner U, Young AB, Penney JB, Beal MF. 1994. 3-nitropropionic acid toxicity in the striatum. J Neurochem 63:1772-1781.