Altered microglia in the amygdala are involved in anxiety-related behaviors of a copy number variation mouse model of autism

Journal of Nippon Medical School

Volumn 82, Issue 2, 2015, Pages 92-99

  Shigemori, Tomoko ^a   Sakai, Atsushi ^a   Takumi, Toru ^b   Itoh, Yasuhiko ^a   Suzuki, Hidenori ^a  

^a NIPPON MEDICAL SCHOOL   (Japan)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Amygdala; Anxiety; Autism spectrum disorder; Microglia; Minocycline

Indexed keywords

ALLOGRAFT INFLAMMATORY FACTOR 1; MINOCYCLINE; ACTIN BINDING PROTEIN; AIF1 PROTEIN, MOUSE; BIOLOGICAL MARKER; CALCIUM BINDING PROTEIN;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY DISORDER; ARTICLE; AUTISM; CHROMOSOME; CONNECTOME; COPY NUMBER VARIATION; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; MICROGLIA; MOUSE; NEWBORN; NONHUMAN; OPEN FIELD TEST; PROTEIN EXPRESSION; SOCIAL BEHAVIOR; TASK PERFORMANCE; AGE; ANIMAL; ANXIETY; AUTISM SPECTRUM DISORDER; C57BL MOUSE; CHROMOSOME DUPLICATION; DISEASE MODEL; DRUG EFFECTS; GENE DOSAGE; GENETIC PREDISPOSITION; GENETICS; MALE; METABOLISM; PATHOLOGY; PHENOTYPE; PSYCHOLOGY; TRANSGENIC MOUSE;

AGE FACTORS; AMYGDALA; ANIMALS; ANIMALS, NEWBORN; ANXIETY; AUTISM SPECTRUM DISORDER; BEHAVIOR, ANIMAL; BIOMARKERS; CALCIUM-BINDING PROTEINS; CHROMOSOME DUPLICATION; CHROMOSOMES, MAMMALIAN; DISEASE MODELS, ANIMAL; DNA COPY NUMBER VARIATIONS; GENE DOSAGE; GENETIC PREDISPOSITION TO DISEASE; MALE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROFILAMENT PROTEINS; MICROGLIA; MINOCYCLINE; PHENOTYPE;

EID: 84928988874     PISSN: 13454676     EISSN: 13473409     Source Type: Journal    
DOI: 10.1272/jnms.82.92     Document Type: Article

References (54)

1. Liu X, Takumi T: Genomic and genetic aspects of autism spectrum disorder. Biochem Biophys Res Commun 2014; in press.
2. Lai MC, Lombardo MV, Baron-Cohen S: Autism. Lancet 2014; 383: 896-910.
3. Geschwind DH, Levitt P: Autism spectrum disorders: developmental disconnection syndromes. Curr Opin Neurobiol 2007; 17: 103-111.
4. Gesundheit B, Rosenzweig JP, Naor D, Lerer B, Zachor DA, Procházka V, Melamed M, Kristt DA, Steinberg A, Shulman C, Hwang P, Koren G, Walfisch A, Passweg JR, Snowden JA, Tamouza R, Leboyer M, Farge-Bancel D, Ashwood P: Immunological and autoimmune considerations of Autism Spectrum Disorders. J Autoimmun 2013; 44: 1-7.
5. van Steensel FJA, Bögels SM, Perrin S: Anxiety disorders in children and adolescents with autistic spectrum disorders: a meta-analysis. Clin Child Fam Psychol Rev 2011; 14: 302-317.
6. Rodgers J, Glod M, Connolly B, McConachie H: The relationship between anxiety and repetitive behaviours in autism spectrum disorder. J Autism Dev Disord 2012; 42: 2404-2409.
7. Eussen ML, Van Gool SR, Verheij F, De Nijs PF, Verhulst FC, Greaves-Lord K: The association of quality of social relations, symptom severity and intelligence with anxiety in children with autism spectrum disorders. Autism 2013; 17: 723-735.
8. Allsop SA, Vander Weele CM, Wichmann R, Tye KM: Optogenetic insights on the relationship between anxietyrelated behaviors and social deficits. Front Behav Neurosci 2014; 8: 241.
9. Baron-Cohen S, Ring HA, Bullmore ET, Wheelwright S, Ashwin C, Williams SCR: The amygdala theory of autism. Neurosci Biobehav Rev 2000; 24: 355-364.
10. Zalla T, Sperduti M: The amygdala and the relevance detection theory of autism: an evolutionary perspective. Front Hum Neurosci 2013; 7: 894.
11. Schumann CM, Nordahl CW: Bridging the gap between MRI and postmortem research in autism. Brain Res 2011; 1380: 175-186.
12. Schumann CM, Hamstra J, Goodlin-Jones BL, Lotspeich LJ, Kwon H, Buonocore MH, Lammers CR, Reiss AL, Amaral DG: The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. J Neurosci 2004; 24: 6392-6401.
13. Breece E, Paciotti B, Nordahl CW, Ozonoff S, Van de Water JA, Rogers SJ, Amaral D, Ashwood P: Myeloid dendritic cells frequencies are increased in children with autism spectrum disorder and associated with amygdala volume and repetitive behaviors. Brain Behav Immun 2012; 31: 69-75.
14. Aylward EH, Minshew NJ, Goldstein G, Honeycutt NA, Augustine AM, Yates KO, Barta PE, Pearlson GD: MRI volumes of amygdala and hippocampus in non-mentally retarded autistic adolescents and adults. Neurology 1999; 53: 2145-2150.
15. Duerden EG, Mak-Fan KM, Taylor MJ, Roberts SW: Regional differences in grey and white matter in children and adults with autism spectrum disorders: an activation likelihood estimate (ALE) meta-analysis. Autism Res 2012; 5: 49-66.
16. Cauda F, Geda E, Sacco K, D’Agata F, Duca S, Geminiani G, Keller R: Grey matter abnormality in autism spectrum disorder: an activation likelihood estimation metaanalysis study. J Neurol Neurosurg Psychiatry 2011; 82: 1304-1313.
17. Via E, Radua J, Cardoner N, Happé F, Mataix-Cols D: Meta-analysis of gray matter abnormalities in autism spectrum disorder: should Asperger disorder be subsumed under a broader umbrella of autistic spectrum disorder? Arch Gen Psychiatry 2011; 68: 409-418.
18. Chanm WY, Kohsaka S, Rezaie P: The origin and cell lineage of microglia- new concepts. Brain Res Rev 2007; 53: 344-354.
19. Kaur C, Hao A-J, Wu C-H, Ling E-A: Origin of microglia. Microsc Res Tech 2001; 54: 2-9.
20. Pont-Lezica L, Bechade C, Belarif-Cantaut Y, Pascual O, Bessis A: Physiological roles of microglia during development. J Neurochem 2011; 119: 901-908.
21. Prinz M, Mildner A: Microglia in the CNS: immigrants from another world. Glia 2011; 59: 177-187.
22. Alliot F, Godin I, Pessac B: Microglia derive from progenitors, originating from the yolk sac, and which proliferate in the brain. Dev Brain Res 1999; 117: 145-152.
23. Wake H, Moorhouse AJ, Miyamoto A, Nabekura J: Microglia: actively surveying and shaping neuronal circuit structure and function. Trends Neurosci 2013; 36: 209-217.
24. Pardo CA, Vargas DL, Zimmerman AW: Immunity, neuroglia and neuroinflammation in autism. Int Rev Psychiatry 2005; 17: 485-495.
25. Vargas DL, Nascimbene C, Krishnan C, Zimmerman AW, Pardo CA: Neurologial activation and neuroinflammation in the brain of patients with autism. Ann Neurol 2005; 57: 67-81.
26. Zimmerman AW, Jyonouchi H, Comi AM, Connors SL, Milstien S, Varsou A, Heyes MP: Cerebrospinal fluid and serum markers of inflammation in autism. Pediatr Neurol 2005; 33: 195-201.
27. Simms ML, Kemper TL, Timbie CM, Bauman ML, Blatt GJ: The anterior cingulate cortex in autism: heterogeneity of qualitative and quantitative cytoarchitectonic features suggests possible subgroups. Acta Neuropathol 2009; 118: 673-684.
28. Morgan JT, Chana G, Pardo CA, Achim C, Semendeferi K, Buckwalter J, Courchesne E, Everall IP: Microglial activation and increased microglial density observed in the dorsolateral prefrontal cortex in autism. Biol Psychiatry 2010; 68: 368-376.
29. Morgan JT, Chana G, Abramson I, Semendeferi K, Courchesne E, Everall IP: Abnormal microglial-neuronal spatial organization in the dorsolateral prefrontal cortex in autism. Brain Res 2012; 1456: 72-81.
30. Tetreault NA, Hakeem AY, Jiang S, Williams BA, Allman E, Wold BJ, Allman JM: Microglia in the cerebral cortex in autism. J Autism Dev Disord 2012; 42: 2569-2584.
31. Mattei D, Djodari-Irani A, Hadar R, Pelz A, de Cossío LF, Goetz T, Matyash M, Kettenmann H, Winter C, Wolf SA: Minocycline rescues decrease in neurogenesis, increase in microglia cytokines and deficits in sensorimotor gating in an animal model of schizophrenia. Brain Behav Immun 2014; 38: 175-184.
32. Zhan Y, Paolicelli RC, Sforazzini F, Weinhard L, Bolasco G, Pagani F, Vyssotski AL, Bifone A, Gozzi A, Ragozzino D, Gross CT: Deficient neuron-microglia signaling results in impaired functional brain connectivity and social behavior. Nat Neurosci 2014; 17: 400-406.
33. Derecki NC, Cronk JC, Lu Z, Xu E, Abbott SB, Guyenet PG, Kipnis J: Wild-type microglia arrest pathology in a mouse model of Rett syndrome. Nature 2012; 484: 105- 109.
34. Nakatani J, Tamada K, Hatanaka F, Ise S, Ohta H, Inoue K, Tomonaga S, Watanabe Y, Chung YJ, Banerjee R, Iwamoto K, Kato T, Okazawa M, Yamauchi K, Tanda K, Takao K, Miyakawa T, Bradley A, Takumi T: Abnormal behavior in a chromosome-engineered mouse model for human 15q11-13 duplication seen in autism. Cell 2009; 137: 1235-1246.
35. Tamada K, Tomonaga S, Hatanaka F, Nakai N, Takao K, Miyakawa T, Nakatani J, Takumi T: Decreased exploratory activity in a mouse model of 15q duplication syndrome; implications for disturbance of serotonin signaling. PLoS One 2010; 5: e15126.
36. Lin S, Wei X, Bales KR, Paul AB, Ma Z, Yan G, Paul SM, Du Y: Minocycline blocks bilirubin neurotoxicity and prevents hyperbilirubinemia-induced cerebellar hypoplasia in the Gunn rat. Eur J Neurosci 2005; 22: 21-27.
37. Luzi P, Abraham RM, Rafi MA, Curtis M, Hooper DC, Wenger DA: Effects of treatments on inflammatory and apoptotic markers in the CNS of mice with globoid cell leukodystrophy. Brain Res 2009; 1300: 146-158.
38. Rotschafer SE, Trujillo MS, Dansie LE, Ethell IM, Razak KA: Minocycline treatment reverses ultrasonic vocalization production deficit in a mouse model of Fragile X Syndrome. Brain Res 2012; 1439: 7-14.
39. Dansie LE, Phommahaxay K, Okusanya AG, Uwadia J, Huang M, Rotschafer SE, Razak KA, Ethell DW, Ethell IM: Long-lasting effects of minocycline on behavior in young but not adult Fragile X mice. Neuroscience 2013; 246: 186-198.
40. Scattoni ML, Crawley J, Ricceri L: Ultrasonic vocalizations: a tool for behavioural phenotyping of mouse models of neurodevelopmental disorders. Neurosci Biobehav Rev 2009; 33: 508-515.
41. Braunschweig D, Golub MS, Koenig CM, Qi L, Pessah IN, Van de Water J, Berman RF: Maternal autism-associated IgG antibodies delay development and produce anxiety in a mouse gestational transfer model. J Neuroimmunol 2012; 252: 56-65.
42. Malkova NV, Yu CZ, Hsiao EY, Moore MJ, Patterson PH: Maternal immune activation yields offspring displaying mouse versions of the three core symptoms of autism. Brain Behav Immun 2012; 26: 607-616.
43. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A: Physiology of microglia. Physiol Rev 2011; 91: 461-553.
44. Brunelli SA, Hofer MA: Selective breeding for infant rat separation-induced ultrasonic vocalizations: Developmental precursors of passive and active coping styles. Behav Brain Res 2007; 182: 193-207.
45. Laloux C, Mairesse J, Van Camp G, Giovine A, Branchi I, Bouret S, Morley-Fletcher S, Bergonzelli G, Malagodi M, Gradini R, Nicoletti F, Darnaudéry M, Maccari S: Anxietylike behaviour and associated neurochemical and endocrinological alterations in male pups exposed to prenatal stress. Psychoneuroendocrinology 2012; 37: 1646-1658.
46. Sasaki A, de Vega WC, St-Cyr S, Pan P, McGowan PO: Perinatal high fat diet alters glucocorticoid signaling and anxiety behavior in adulthood. Neuroscience 2013; 240: 1- 12.
47. Nagano M, Ozawa H, Suzuki H: Prenatal dexamethasone exposure affects anxiety-like behaviour and neuroendocrine systems in an age-dependent manner. Neurosci Res 2008; 60: 364-371.
48. Schumann CM, Amaral DG: Stereological analysis of amygdala neuron number in autism. J Neurosci 2006; 26: 7674-7679.
49. Monk CS, Weng SJ, Wiggins JL, Kurapati N, Louro HM, Carrasco M, Maslowsky J, Risi S, Lord C: Neural circuitry of emotional face processing in autism spectrum disorders. J Psychiatry Neurosci 2010; 35: 105-114.
50. Paolicelli RC, Gross CT: Microglia in development: linking brain wiring to brain environment. Neuron Glia Biol 2011; 7: 77-83.
51. Maezawa I, Calafiore M, Wulff H, Jin L-W: Does microglial dysfunction play a role in autism and Rett syndrome? Neuron Glia Biol 2011; 7: 85-97.
52. Stephenson DT, O’Neill SM, Narayan S, Tiwari A, Arnold E, Samaroo HD, Du F, Ring RH, Campbell B, Pletcher M, Vaidya VA, Morton D: Histopathologic characterization of the BTBR mouse model of autistic-like behavior reveals selective changes in neurodevelopmental proteins and adult hippocampal neurogenesis. Mol Autism 2011; 2: 7.
53. Maezawa I, Jin L-W: Rett syndrome microglia damage dendrites and synapses by the elevated release of glutamate. J Neuroscience 2010; 30: 5346-5356.
54. Bilousova TV, Dansie L, Ngo M, Aye J, Charles JR, Ethell DW, Ethell IM: Minocycline promotes dendritic spine maturation and improves behavioural performance in the fragile X mouse model. J Med Genet 2009; 46: 94-102.