Developmental disruption of perineuronal nets in the medial prefrontal cortex after maternal immune activation

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Paylor, John W ^a   Lins, Brittney R ^b   Greba, Quentin ^b   Moen, Nicholas ^a   De Moraes, Reiner Silveira ^a   Howland, John G ^b   Winship, Ian R ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; PARVALBUMIN; POLYINOSINIC POLYCYTIDYLIC ACID;

ANIMAL; ASTROCYTE; DRUG EFFECT; FEMALE; IMMUNITY; IMMUNOLOGY; LONG EVANS RAT; METABOLISM; MICROGLIA; PREFRONTAL CORTEX; PREGNANCY;

ANIMALS; ASTROCYTES; BIOMARKERS; FEMALE; IMMUNITY; MICROGLIA; PARVALBUMINS; POLY I-C; PREFRONTAL CORTEX; PREGNANCY; RATS, LONG-EVANS;

EID: 84996774899     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep37580     Document Type: Article

References (81)

1. Eaton, W. W. et al. The burden of mental disorders. Epidemiol. Rev. 30, 1-4 (2008).
2. Mathers, C., Fat, D. M. & Boerma, J. T. The global burden of disease: 2004 update. World Health Organization (2008).
3. Brown, A. S. & Derkits, E. J. Prenatal infection and schizophrenia: a review of epidemiologic and translational studies. Am. J. Psychiatry 167, 261-280 (2010).
4. Brown, A. S. Epidemiologic studies of exposure to prenatal infection and risk of schizophrenia and autism. Dev. Neurobiol 72, 1272-1276 (2012).
5. Meyer, U. & Feldon, J. To poly (I: C) or not to poly (I: C): advancing preclinical schizophrenia research through the use of prenatal immune activation models. Neuropharmacology 62, 1308-1321 (2012).
6. Meyer, U., Feldon, J. & Fatemi, S. H. In-vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders. Neurosci. Biobehav. Rev. 33, 1061-1079 (2009).
7. Meyer, U. Prenatal poly (i: C) exposure and other developmental immune activation models in rodent systems. Biol. Psychiatry 75, 307-315 (2014).
8. Dickerson, D. D., Wolff, A. R. & Bilkey, D. K. Abnormal long-range neural synchrony in a maternal immune activation animal model of schizophrenia. J. Neurosci 30, 12424-12431 (2010).
9. Dickerson, D. D. et al. Association of aberrant neural synchrony and altered GAD67 expression following exposure to maternal immune activation, a risk factor for schizophrenia. Transl. Psychiatry 4, e418, doi: 10.1038/tp.2014.64 (2014).
10. Howland, J. G., Cazakoff, B. N. & Zhang, Y. Altered object-in-place recognition memory, prepulse inhibition, and locomotor activity in the offspring of rats exposed to a viral mimetic during pregnancy. Neuroscience 201, 184-198 (2012).
11. Piontkewitz, Y., Arad, M. & Weiner, I. Tracing the development of psychosis and its prevention: what can be learned from animal models. Neuropharmacology 62, 1273-1289 (2012).
12. Zhang, Y., Cazakoff, B. N., Thai, C. A. & Howland, J. G. Prenatal exposure to a viral mimetic alters behavioural flexibility in male, but not female, rats. Neuropharmacology 62, 1299-1307 (2012).
13. Sangha, S., Greba, Q., Robinson, P. D., Ballendine, S. A. & Howland, J. G. Heightened fear in response to a safety cue and extinguished fear cue in a rat model of maternal immune activation. Front. Behav. Neurosci. 8, 168 (2014).
14. Ballendine, S. A. et al. Behavioral alterations in rat offspring following maternal immune activation and ELR-CXC chemokine receptor antagonism during pregnancy: implications for neurodevelopmental psychiatric disorders. Prog. Neuropsychopharmacol. Biol. Psychiatry 57, 155-165 (2015).
15. Machado, C. J., Whitaker, A. M., Smith, S. E., Patterson, P. H. & Bauman, M. D. Maternal immune activation in nonhuman primates alters social attention in juvenile offspring. Biol. Psychiatry 77, 823-832 (2015).
16. Berretta, S., Pantazopoulos, H., Markota, M., Brown, C. & Batzianouli, E. T. Losing the sugar coating: potential impact of perineuronal net abnormalities on interneurons in schizophrenia. Schizophr Res. 167, 18-27 (2015).
17. Do, K. Q., Cuenod, M. & Hensch, T. K. Targeting oxidative stress and aberrant critical period plasticity in the developmental trajectory to schizophrenia. Schizophr. Bull. 10.1093/schbul/sbv065 (2015).
18. Hockfield, S., Kalb, R. G., Zaremba, S. & Fryer, H. Expression of neural proteoglycans correlates with the acquisition of mature neuronal properties in the mammalian brain. Cold Spring Harb. Symp. Quant. Bio. 55, 505-514 (1990).
19. Bruckner, G. et al. Perineuronal nets provide a polyanionic, glia-associated form of microenvironment around certain neurons in many parts of the rat brain. Glia, 8, 183-200 (1993).
20. Bruckner, G., Bringmann, A., Koppe, G., Hartig, W. & Brauer, K. In vivo and in vitro labelling of perineuronal nets in rat brain. Brain Res. 720, 84-92 (1996).
21. Koppe, G., Bruckner, G., Hartig, W., Delpech, B. & Bigl, V. Characterization of proteoglycan-containing perineuronal nets by enzymatic treatments of rat brain sections. Histochem. J. 29, 11-20 (1997).
22. Hartig, W. et al. Perineuronal nets in the rat medial nucleus of the trapezoid body surround neurons immunoreactive for various amino acids, calcium-binding proteins and the potassium channel subunit Kv3. 1b. Brain Res. 899, 123-133 (2001).
23. Fox, K. & Caterson, B. Freeing the brain from the perineuronal net. Science 298, 1187-1189 (2002).
24. Pizzorusso, T. et al. Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298, 1248-1251 (2002).
25. Berardi, N., Pizzorusso, T., Ratto, G. M. & Maffei, L. Molecular basis of plasticity in the visual cortex. Trends Neurosci. 26, 369-378 (2003).
26. Rhodes, K. E. & Fawcett, J. W. Chondroitin sulphate proteoglycans: preventing plasticity or protecting the CNS? J. Anat. 204, 33-48 (2004).
27. Pantazopoulos, H., Woo, T. U., Lim, M. P., Lange, N. & Berretta, S. Extracellular matrix-glial abnormalities in the amygdala and entorhinal cortex of subjects diagnosed with schizophrenia. Arch. Gen. Psychiatry 67, 155-166 (2010).
28. Pantazopoulos, H. et al. Proteoglycan abnormalities in olfactory epithelium tissue from subjects diagnosed with schizophrenia. Schizophr. Res. 150, 366-372 (2013).
29. Pantazopoulos, H. et al. Aggrecan and chondroitin-6-sulfate abnormalities in schizophrenia and bipolar disorder: a postmortem study on the amygdala. Transl. Psychiatry 5, e496, doi: 10.1038/tp.2014.128 (2015).
30. Mauney, S. A. et al. Developmental pattern of perineuronal nets in the human prefrontal cortex and their deficit in schizophrenia. Biol. Psychiatry 74, 427-435 (2013).
31. Enwright, J. F. et al. Reduced Labeling of Parvalbumin Neurons and Perineuronal Nets in the Dorsolateral Prefrontal Cortex of Subjects with Schizophrenia. Neuropsychopharmacology 41, 2206-2214 (2016).
32. Bitanihirwe, B. K. & Woo, T. U. Perineuronal nets and schizophrenia: the importance of neuronal coatings. Neurosci. Biobehav. Rev. 45, 85-99 (2014).
33. Sur, M., Frost, D. O. & Hockfield, S. Expression of a surface-associated antigen on Y-cells in the cat lateral geniculate nucleus is regulated by visual experience. J. Neurosci. 8, 874-882 (1988).
34. Bavelier, D., Levi, D. M., Li, R. W., Dan, Y. & Hensch T. K. Removing brakes on adult brain plasticity: from molecular to behavioral interventions. J. Neurosci. 30, 14964-14971 (2010).
35. Takesian, A. E. & Hensch, T. K. Balancing plasticity/stability across brain development. Prog. Brain Res. 207, 3-4 (2013).
36. Tukker, J. J., Fuentealba, P., Hartwich, K., Somogyi, P. & Klausberger T. Cell type-specific tuning of hippocampal interneuron firing during gamma oscillations in vivo. J. Neurosci. 27, 8184-8189 (2007).
37. Sohal, V. S., Zhang, F., Yizhar, O. & Deisseroth, K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature, 459, 698-702 (2009).
38. Buzsaki, G. & Wang, X. J. Mechanisms of gamma oscillations. Ann. Rev. Neurosci. 35, 203 (2012).
39. Hashimoto, T. et al. Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia J. Neurosci. 23, 6315-6326 (2003).
40. Cho, R. Y., Konecky, R. O. & Carter, C. S. Impairments in frontal cortical γ synchrony and cognitive control in schizophrenia. Proc. Natl. Acad. Sci. USA 103, 19878-19883 (2006).
41. Basar-Eroglu, C. et al. Working memory related gamma oscillations in schizophrenia patients. Int. J. Psychophysiol. 64, 39-45 (2007).
42. Mellios, N. et al. Molecular determinants of dysregulated GABAergic gene expression in the prefrontal cortex of subjects with schizophrenia. Biol. Psychiatry 65, 1006-1014 (2009).
43. Spencer, K. M., Niznikiewicz, M. A., Shenton, M. E. & McCarley, R. W. Sensory-evoked gamma oscillations in chronic schizophrenia. Biol. Psychiatry 63, 744-747 (2008).
44. Fung, S. J. et al. Expression of interneuron markers in the dorsolateral prefrontal cortex of the developing human and in schizophrenia. Am. J. Psychiatry 167, 1479-1488 (2010).
45. Gonzalez-Burgos, G., Hashimoto, T. & Lewis, D. A. Alterations of cortical GABA neurons and network oscillations in schizophrenia. Curr. Psychiatry Rep. 12, 335-344 (2010).
46. Hartig, W. et al. Cortical neurons immunoreactive for the potassium channel Kv3. 1b subunit are predominantly surrounded by perineuronal nets presumed as a buffering system for cations. Brain Res. 842, 15-29 (1999).
47. Reinert, T., Morawski, M., Arendt, T. & Butz, T. Quantitative microanalysis of perineuronal nets in brain tissue. Nucl. Instrum. Methods Phys. Res. B. 210, 395-400 (2003).
48. Lewis, D. A., Curley, A. A., Glausier, J. R. & Volk, D. W. Cortical parvalbumin interneurons and cognitive dysfunction in schizophrenia. Trends Neurosci. 35, 57-67 (2012).
49. Gonzalez-Burgos, G., Cho, R. Y. & Lewis, D. A. Alterations in cortical network oscillations and parvalbumin neurons in schizophrenia. Biol. Psychiatry 77, 1031-1040 (2015).
50. Curley, A. A. & Lewis, D. A. Cortical basket cell dysfunction in schizophrenia. J. Physiology 590, 715-724 (2012).
51. Volk, D. W. et al. Deficits in transcriptional regulators of cortical parvalbumin neurons in schizophrenia. Am. J. Psychiatry 169, 1082-1091 (2012).
52. Glausier, J. R., Fish, K. N. & Lewis, D. A. Altered parvalbumin basket cell inputs in the dorsolateral prefrontal cortex of schizophrenia subjects. Mol. Psychiatry 19, 30-36 (2014).
53. Richetto, J., Calabrese, F., Riva, M. A. & Meyer, U. Prenatal immune activation induces maturation-dependent alterations in the prefrontal GABAergic transcriptome. Schizophr. Bull 40, 51-61 (2014).
54. Cassella, S. N. et al. Maternal immune activation alters glutamic acid decarboxylase-67 expression in the brains of adult rat offspring. Schizophr. Res. 171, 195-199 (2016).
55. Canetta, S. et al. Maternal immune activation leads to selective functional deficits in offspring parvalbumin interneurons. Mol. Psychiatry 21, 956-968 (2016).
56. Zahrt, J., Taylor, J. R., Mathew, R. G. & Arnsten, A. F. Supranormal stimulation of D1 dopamine receptors in the rodent prefrontal cortex impairs spatial working memory performance. J. Neurosci. 17, 8528-8535 (1997).
57. Miner, L. A., Ostrander, M. & Sarter, M. Effects of ibotenic acid-induced loss of neurons in the medial prefrontal cortex of rats on behavioral vigilance: evidence for executive dysfunction. J. Psychopharmacol. 11, 169-178 (1997).
58. Passetti, F., Chudasama, Y. & Robbins, T. W. The frontal cortex of the rat and visual attentional performance: dissociable functions of distinct medial prefrontal subregions. Cereb. Cortex 12, 1254-1268 (2002).
59. Wolff, A. R. & Bilkey, D. K. Immune activation during mid-gestation disrupts sensorimotor gating in rat offspring. Behav. Brain Res. 190, 156-159 (2008).
60. Wolff, A. R., Cheyne, K. R. & Bilkey, D. K. Behavioural deficits associated with maternal immune activation in the rat model of schizophrenia. Behav. Brain Res. 225, 382-387 (2011).
61. Li, W. Y., Chang, Y. C., Lee, L. H. & Lee, L. J. Prenatal infection affects the neuronal architecture and cognitive function in adult mice. Dev. Neurosci. 36, 359-370 (2014).
62. Vorhees, C. V. et al. Prenatal immune challenge in rats: effects of polyinosinic-polycytidylic acid on spatial learning, prepulse inhibition, conditioned fear, and responses to MK-801 and amphetamine. Neurotoxicol. Teratol. 47, 54-65 (2015).
63. Malkova, N. V., Yu, C. Z., Hsiao, E. Y., Moore, M. J. & Patterson, P. H. Maternal immune activation yields offspring displaying mouse versions of three core symptoms of autism. Brain Behav. Immun. 26, 607-616 (2012).
64. Wang, D. & Fawcett, J. The perineuronal net and the control of CNS plasticity. Cell Tissue Res. 349, 147-160 (2012).
65. Bitanihirwe, B. K., Mauney, S. A. & Woo, T. U. Weaving a Net of Neurobiological Mechanisms in Schizophrenia and Unraveling the Underlying Pathophysiology. Biol. Psychiatry, doi: 10.1016/j.biopsych.2016.03.1047 (2016).
66. Pantazopoulos, H. & Berretta, S. In Sickness and in Health: Perineuronal Nets and Synaptic Plasticity in Psychiatric Disorders. Neural Plast. doi: 10.1155/2016/9847696 (2016).
67. Gogolla, N., Caroni, P., Luthi, A. & Herry, C. Perineuronal nets protect fear memories from erasure. Science 325, 1258-1261 (2009).
68. Ibi, D. et al. Combined effect of neonatal immune activation and mutant DISC1 on phenotypic changes in adulthood. Behav. Brain Res. 206, 32-37 (2010).
69. Beasley, C. L. & Reynolds, G. P. Parvalbumin-immunoreactive neurons are reduced in the prefrontal cortex of schizophrenics. Schizophr. Res. 24, 349-355 (1997).
70. Nakayama, D. et al. Frontal association cortex is engaged in stimulus integration during associative learning. Curr. Biol. 25, 117-123 (2015).
71. Faissner, A. et al. Contributions of astrocytes to synapse formation and maturation - potential functions of the perisynaptic extracellular matrix. Brain Res. Rev. 63, 26-38 (2010).
72. Wiese, S., Karus, M. & Faissner, A. Astrocytes as a source for extracellular matrix molecules and cytokines. Front. Pharmacol. 3, 120 (2012).
73. Gottschall, P. E. & Deb, S. Regulation of matrix metalloproteinase expression in astrocytes, microglia and neurons. Neuroimmunomodulation, 3, 69-75 (1996).
74. Klausmeyer, A., Conrad, R., Faissner, A. & Wiese, S. Influence of glial-derived matrix molecules, especially chondroitin sulfates, on neurite growth and survival of cultured mouse embryonic motorneurons. J. Neurosci. Res. 89, 127-141 (2011).
75. Giovanoli, S., Weber-Stadlbauer, U., Schedlowski, M., Meyer, U. & Engler, H. Prenatal immune activation causes hippocampal synaptic deficits in the absence of overt microglia anomalies. Brain Behav. Immun. 55, 25-38 (2016).
76. Smolders, S. et al. Maternal immune activation evoked by polyinosinic: polycytidylic acid does not evoke microglial cell activation in the embryo. Front. Cell Neurosci. 9, 301 (2015).
77. Domenici, E. et al. Plasma protein biomarkers for depression and schizophrenia by multi analyte profiling of case-control collections. PLoS One 5, e9166 (2010).
78. Yamamori, H. et al. Plasma levels of mature brain-derived neurotrophic factor (BDNF) and matrix metalloproteinase-9 (MMP-9) in treatment-resistant schizophrenia treated with clozapine. Neurosci. Lett. 556, 37-41 (2013).
79. Pietersen, C. Y. et al. Molecular profiles of parvalbumin-immunoreactive neurons in the superior temporal cortex in schizophrenia. J. Neurogenet. 28, 70-85 (2014).
80. Devanarayanan, S., Nandeesha, H., Kattimani, S. & Sarkar, S. Relationship between matrix metalloproteinase-9 and oxidative stress in drug-free male schizophrenia: a case control study. Clin. Chem. Lab Med. 54, 447-452 (2016).
81. Paxinos, G. & Watson, C. The rat brain atlas in stereotaxic coordinates. San Diego: Academic (1998).