Activation of mGluR2/3 underlies the effects of N-acetylcystein on amygdala-associated autism-like phenotypes in a valproate-induced rat model of autism

Frontiers in Behavioral Neuroscience

Volumn 8, Issue JUNE, 2014, Pages

  Chen, Yu Wen ^a   Lin, Hui Ching ^b   Ng, Ming Chong ^a   Hsiao, Ya Hsin ^a   Wang, Chao Chuan ^c   Gean, Po Wu ^a   Chen, Po See ^a,d  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^d NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

Amygdala; Autistic spectrum disorders; Glutamate; N acetylcysteine; Valproate

Indexed keywords

ACETYLCYSTEINE; METABOTROPIC RECEPTOR 2; METABOTROPIC RECEPTOR 3;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; AUTISM; CONTROLLED STUDY; ELEVATED PLUS MAZE TEST; FACILITATION; MGLUR2 GENE; MGLUR3 GENE; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; OPEN FIELD TEST; PHENOTYPE; PRESYNAPTIC POTENTIAL; PROTEIN EXPRESSION; RAT; SOCIAL INTERACTION; SOCIAL INTERACTION TEST; SYNAPSE; THALAMUS NUCLEUS; TRANQUILIZING ACTIVITY;

EID: 84902591233     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00219     Document Type: Article

References (48)

1. Adolphs, R., Tranel, D., and Damasio, H. (2001). Emotion recognition from faces and prosody following temporal lobectomy. Neuropsychology 15, 396-404. doi: 10.1037/0894-4105.15.3.396
2. Aylward, E. H., Minshew, N. J., Goldstein, G., Honeycutt, N. A., Augustine, A. M., Yates, K. O., et al. (1999). MRI volumes of amygdala and hippocampus in non-mentally retarded autistic adolescents and adults. Neurology 53, 2145-2150. doi: 10.1212/WNL.53.9.2145
3. Baharnoori, M., Bhardwaj, S. K., and Srivastava, L. K. (2012). Neonatal behavioral changes in rats with gestational exposure to lipopolysaccharide: a prenatal infection model for developmental neuropsychiatric disorders. Schizophr. Bull. 38, 444-456. doi: 10.1093/schbul/sbq098
4. Bailey, A., Luthert, P., Dean, A., Harding, B., Janota, I., Montgomery, M., et al. (1998). A clinicopathological study of autism. Brain 121(pt 5), 889-905. doi: 10.1093/brain/121.5.889
5. Baird, G., Simonoff, E., Pickles, A., Chandler, S., Loucas, T., Meldrum, D., et al. (2006). Prevalence of disorders of the autism spectrum in a population cohort of children in South Thames: the Special Needs and Autism Project (SNAP). Lancet 368, 210-215. doi: 10.1016/S0140-6736(06) 69041-7
6. Baker, D. A., Xi, Z. X., Shen, H., Swanson, C. J., and Kalivas, P. W. (2002). The origin and neuronal function of in vivo nonsynaptic glutamate. J. Neurosci. 22, 9134-9141.
7. Baron-Cohen, S., and Belmonte, M. K. (2005). Autism: a window onto the development of the social and the analytic brain. Annu. Rev. Neurosci. 28, 109-126. doi: 10.1146/annurev.neuro.27.070203.144137
8. Baron-Cohen, S., Ring, H. A., Bullmore, E. T., Wheelwright, S., Ashwin, C., and Williams, S. C. (2000). The amygdala theory of autism. Neurosci. Biobehav. Rev. 24, 355-364. doi: 10.1016/S0149-7634(00)00011-7
9. Baron-Cohen, S., Ring, H. A., Wheelwright, S., Bullmore, E. T., Brammer, M. J., Simmons, A., et al. (1999). Social intelligence in the normal and autistic brain: an fMRI study. Eur. J. Neurosci. 11, 1891-1898. doi: 10.1046/j.14609568.1999.00621.x
10. Bateup, H. S., Johnson, C. A., Denefrio, C. L., Saulnier, J. L., Kornacker, K., and Sabatini, B. L. (2013). Excitatory/inhibitory synaptic imbalance leads to hippocampal hyperexcitability in mouse models of tuberous sclerosis. Neuron 78, 510-522. doi: 10.1016/j.neuron.2013.03.017
11. Christensen, J., Gronborg, T. K., Sorensen, M. J., Schendel, D., Parner, E. T., Pedersen, L. H., et al. (2013). Prenatal valproate exposure and risk of autism spectrum disorders and childhood autism. JAMA 309, 1696-1703. doi: 10.1001/jama.2013.2270
12. Dalton, K. M., Nacewicz, B. M., Johnstone, T., Schaefer, H. S., Gernsbacher, M. A., Goldsmith, H. H., et al. (2005). Gaze fixation and the neural circuitry of face processing in autism. Nat. Neurosci. 8, 519-526. doi: 10.1038/nn1421
13. Eichler, S. A., and Meier, J. C. (2008). E-I balance and human diseases-from molecules to networking. Front. Mol. Neurosci. 1:2. doi: 10.3389/neuro.02.002.2008
14. El-Ansary, A. K., Ben Bacha, A., and Kotb, M. (2012). Etiology of autistic features: the persisting neurotoxic effects of propionic acid. J. Neuroinflammation 9:74. doi: 10.1186/1742-2094-9-74
15. Farr, S. A., Poon, H. F., Dogrukol-Ak, D., Drake, J., Banks, W. A., Eyerman, E., et al. (2003). The antioxidants alpha-lipoic acid and N-acetylcysteine reverse memory impairment and brain oxidative stress in aged SAMP8 mice. J. Neurochem. 84, 1173-1183. doi: 10.1046/j.1471-4159.2003.01580.x
16. Flagstad, P., Mork, A., Glenthoj, B. Y., Van Beek, J., Michael-Titus, A. T., and Didriksen, M. (2004). Disruption of neurogenesis on gestational day 17 in the rat causes behavioral changes relevant to positive and negative schizophrenia symptoms and alters amphetamine-induced dopamine release in nucleus accumbens. Neuropsychopharmacology 29, 2052-2064. doi: 10.1038/sj.npp.1300516
17. Foley, K. A., Ossenkopp, K. P., Kavaliers, M., and Macfabe, D. F. (2014). Pre-and neonatal exposure to lipopolysaccharide or the enteric metabolite, propionic acid, alters development and behavior in adolescent rats in a sexually dimorphic manner. PLoS ONE 9:e87072. doi: 10.1371/journal.pone.0087072
18. Fu, A. L., Dong, Z. H., and Sun, M. J. (2006). Protective effect of N-acetyl-L-cysteine on amyloid beta-peptide-induced learning and memory deficits in mice. Brain Res. 1109, 201-206. doi: 10.1016/j.brainres.2006.06.042
19. Gkogkas, C. G., Khoutorsky, A., Ran, I., Rampakakis, E., Nevarko, T., Weatherill, D. B., et al. (2013). Autism-related deficits via dysregulated eIF4E-dependent translational control. Nature 493, 371-377. doi: 10.1038/nature 11628
20. Hadjikhani, N., Joseph, R. M., Snyder, J., and Tager-Flusberg, H. (2007). Abnormal activation of the social brain during face perception in autism. Hum. Brain Mapp. 28, 441-449. doi: 10.1002/hbm.20283
21. Hardan, A. Y., Fung, L. K., Libove, R. A., Obukhanych, T. V., Nair, S., Herzenberg, L. A., et al. (2012). A randomized controlled pilot trial of oral N-acetylcysteine in children with autism. Biol. Psychiatry 71, 956-961. doi: 10.1016/j.biopsych.2012.01.014
22. Hascup, E. R., Hascup, K. N., Pomerleau, F., Huettl, P., Hajos-Korcsok, E., Kehr, J., et al. (2012). An allosteric modulator of metabotropic glutamate receptors (mGluR(2)), (+)-TFMPIP, inhibits restraint stress-induced phasic glutamate release in rat prefrontal cortex. J. Neurochem. 122, 619-627. doi: 10.1111/j.1471-4159.2012.07784.x
23. Hsia, A. Y., Malenka, R. C., and Nicoll, R. A. (1998). Development of excitatory circuitry in the hippocampus. J. Neurophysiol. 79, 2013-2024.
24. Kalivas, P. W. (2009). The glutamate homeostasis hypothesis of addiction. Nat. Rev. Neurosci. 10, 561-572. doi: 10.1038/nrn2515
25. Khan, M., Sekhon, B., Jatana, M., Giri, S., Gilg, A. G., Sekhon, C., et al. (2004). Administration of N-acetylcysteine after focal cerebral ischemia protects brain and reduces inflammation in a rat model of experimental stroke. J. Neurosci. Res. 76, 519-527. doi: 10.1002/jnr.20087
26. Kupchik, Y. M., Moussawi, K., Tang, X. C., Wang, X., Kalivas, B. C., Kolokithas, R., et al. (2012). The effect of N-acetylcysteine in the nucleus accumbens on neurotransmission and relapse to cocaine. Biol. Psychiatry 71, 978-986. doi: 10.1016/j.biopsych.2011.10.024
27. Levitt, P., and Campbell, D. B. (2009). The genetic and neurobiologic compass points toward common signaling dysfunctions in autism spectrum disorders. J. Clin. Invest. 119, 747-754. doi: 10.1172/JCI37934
28. Lin, H. C., Gean, P. W., Wang, C. C., Chan, Y. H., and Chen, P. S. (2013). The amygdala excitatory/inhibitory balance in a valproate-induced rat autism model. PLoS ONE 8:e55248. doi: 10.1371/journal.pone.0055248
29. Macfabe, D. F., Cain, D. P., Rodriguez-Capote, K., Franklin, A. E., Hoffman, J. E., Boon, F., et al. (2007). Neurobiological effects of intraventricular propionic acid in rats: possible role of short chain fatty acids on the pathogenesis and characteristics of autism spectrum disorders. Behav. Brain Res. 176, 149-169. doi: 10.1016/j.bbr.2006.07.025
30. Markram, K., Rinaldi, T., La Mendola, D., Sandi, C., and Markram, H. (2008). Abnormal fear conditioning and amygdala processing in an animal model of autism. Neuropsychopharmacology 33, 901-912. doi: 10.1038/sj.npp. 1301453
31. Nacewicz, B. M., Dalton, K. M., Johnstone, T., Long, M. T., McAuliff, E. M., Oakes, T. R., et al. (2006). Amygdala volume and nonverbal social impairment in adolescent and adult males with autism. Arch. Gen. Psychiatry 63, 1417-1428. doi: 10.1001/archpsyc.63.12.1417
32. Ornstein, P. L., Bleisch, T. J., Arnold, M. B., Kennedy, J. H., Wright, R. A., Johnson, B. G., et al. (1998). 2-substituted (2SR)-2-amino-2-((1SR,2SR)-2-carboxycycloprop-1-yl)glycines as potent and selective antagonists of group II metabotropic glutamate receptors. 2. Effects of aromatic substitution, pharmacological characterization, and bioavailability. J. Med. Chem. 41, 358-378. doi: 10.1021/jm970498o
33. Palmer, R. F., Blanchard, S., and Wood, R. (2009). Proximity to point sources of environmental mercury release as a predictor of autism prevalence. Health Place 15, 18-24. doi: 10.1016/j.healthplace.2008.02.001
34. Parachikova, A., Green, K. N., Hendrix, C., and Laferla, F. M. (2010). Formulation of a medical food cocktail for Alzheimer's disease: beneficial effects on cognition and neuropathology in a mouse model of the disease. PLoS ONE 5:e14015. doi: 10.1371/journal.pone.0014015
35. Reissner, K. J., and Kalivas, P. W. (2010). Using glutamate homeostasis as a target for treating addictive disorders. Behav. Pharmacol. 21, 514-522. doi: 10.1097/FBP.0b013e32833d41b2
36. Roberts, E. M., English, P. B., Grether, J. K., Windham, G. C., Somberg, L., and Wolff, C. (2007). Maternal residence near agricultural pesticide applications and autism spectrum disorders among children in the California Central Valley. Environ. Health Perspect. 115, 1482-1489. doi: 10.1289/ehp.10168
37. Rojas, D. C., Smith, J. A., Benkers, T. L., Camou, S. L., Reite, M. L., and Rogers, S. J. (2004). Hippocampus and amygdala volumes in parents of children with autistic disorder. Am. J. Psychiatry 161, 2038-2044. doi: 10.1176/appi.ajp.161.11.2038
38. Santini, E., Huynh, T. N., Macaskill, A. F., Carter, A. G., Pierre, P., Ruggero, D., et al. (2013). Exaggerated translation causes synaptic and behavioural aberrations associated with autism. Nature 493, 411-415. doi: 10.1038/nature 11782
39. Schumann, C. M., and Amaral, D. G. (2006). Stereological analysis of amygdala neuron number in autism. J. Neurosci. 26, 7674-7679. doi: 10.1523/JNEUROSCI.1285-06.2006
40. Shultz, S. R., Macfabe, D. F., Martin, S., Jackson, J., Taylor, R., Boon, F., et al. (2009). Intracerebroventricular injections of the enteric bacterial metabolic product propionic acid impair cognition and sensorimotor ability in the Long-Evans rat: further development of a rodent model of autism. Behav. Brain Res. 200, 33-41. doi: 10.1016/j.bbr.2008.12.023
41. Todd, R. M., and Anderson, A. K. (2009). Six degrees of separation: the amygdala regulates social behavior and perception. Nat. Neurosci. 12, 1217-1218. doi: 10.1038/nn1009-1217
42. Tyzio, R., Nardou, R., Ferrari, D. C., Tsintsadze, T., Shahrokhi, A., Eftekhari, S., et al. (2014). Oxytocin-mediated GABA inhibition during delivery attenuates autism pathogenesis in rodent offspring. Science 343, 675-679. doi: 10.1126/science.1247190
43. Wang, A. T., Dapretto, M., Hariri, A. R., Sigman, M., and Bookheimer, S. Y. (2004). Neural correlates of facial affect processing in children and adolescents with autism spectrum disorder. J. Am. Acad. Child Adolesc. Psychiatry 43, 481-490. doi: 10.1097/00004583-200404000-00015
44. Wang, C. C., Lin, H. C., Chan, Y. H., Gean, P. W., Yang, Y. K., and Chen, P. S. (2013). 5-HT1A-receptor agonist modified amygdala activity and amygdale-associated social behavior in a valproate-induced rat autism model. Int. J. Neuropsychopharmacol. 16, 2027-2039. doi: 10.1017/S1461145713000473
45. Washburn, M. S., and Moises, H. C. (1992). Electrophysiological and morphological properties of rat basolateral amygdaloid neurons in vitro. J. Neurosci. 12, 4066-4079.
46. Windham, G. C., Zhang, L., Gunier, R., Croen, L. A., and Grether, J. K. (2006). Autism spectrum disorders in relation to distribution of hazardous air pollutants in the san francisco bay area. Environ. Health Perspect. 114, 1438-1444. doi: 10.1289/ehp.9120
47. Wood, A. (in press). Prenatal exposure to sodium valproate is associated with increased risk of childhood autism and autistic spectrum disorder. Evid. Based Nurs. doi: 10.1136/eb-2013-101422
48. Zucker, R. S., and Regehr, W. G. (2002). Short-term synaptic plasticity. Annu. Rev. Physiol. 64, 355-405. doi: 10.1146/annurev.physiol.64.092501.114547