Impaired microglia process dynamics post-stroke are specific to sites of secondary neurodegeneration

Article


Kluge, Murielle G., Kracht, Laura, Mahmoud Abdolhoseini, Ong, Lin Kooi, Johnson, Sarah J., Nilsson, Michael and Walker, Frederick R.. 2017. "Impaired microglia process dynamics post-stroke are specific to sites of secondary neurodegeneration." Glia. 65 (12), pp. 1885-1899. https://doi.org/10.1002/glia.23201
Article Title

Impaired microglia process dynamics post-stroke are specific to sites of secondary neurodegeneration

ERA Journal ID13155
Article CategoryArticle
AuthorsKluge, Murielle G., Kracht, Laura, Mahmoud Abdolhoseini, Ong, Lin Kooi, Johnson, Sarah J., Nilsson, Michael and Walker, Frederick R.
Journal TitleGlia
Journal Citation65 (12), pp. 1885-1899
Number of Pages15
YearDec 2017
Place of PublicationUnited States
ISSN0894-1491
1098-1136
Digital Object Identifier (DOI)https://doi.org/10.1002/glia.23201
Web Address (URL)https://onlinelibrary.wiley.com/doi/10.1002/glia.23201
Abstract

Stroke induces tissue death both at the site of infarction and at secondary sites connected to the primary infarction. This latter process has been referred to as secondary neurodegeneration (SND). Using predominantly fixed tissue analyses, microglia have been implicated in regulating the initial response at both damage sites post-stroke. In this study, we used acute slice based multiphoton imaging, to investigate microglia dynamic process movement in mice 14 days after a photothrombotic stroke. We evaluated the baseline motility and process responses to locally induced laser damage in both the peri-infarct (PI) territory and the ipsilateral thalamus, a major site of post-stroke SND. Our findings show that microglia process extension toward laser damage within the thalamus is lost, yet remains robustly intact within the PI territory. However, microglia at both sites displayed an activated morphology and elevated levels of commonly used activation markers (CD68, CD11b), indicating that the standardly used fixed tissue metrics of microglial “activity” are not necessarily predictive of microglia function. Analysis of the purinergic P2Y12 receptor, a key regulator of microglia process extension, revealed an increased somal localization on nonresponsive microglia in the thalamus. To our knowledge, this is the first study to identify a non-responsive microglia phenotype specific to areas of SND post-stroke, which cannot be identified by the classical assessment of microglia activation but rather the localization of P2Y12 to the soma.

Keywordslaser injury; live cell multiphoton imaging; P2Y12 receptor; peri-infarct; thalamus
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Byline AffiliationsUniversity of Newcastle
Hunter Medical Research Institute, Australia
University of Groningen, Netherlands
NHMRC Centre of Research Excellence Stroke Rehabilitation and Brain Recovery, Australia
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Ong, Lin Kooi, Guan, Liying, Damanhuri, Hanafi, Goodchild, Ann K., Bobrovskaya, Larisa, Dickson, Phillip W. and Dunkley, Peter R.. 2014. "Neurobiological consequences of acute footshock stress: effects on tyrosine hydroxylase phosphorylation and activation in the rat brain and adrenal medulla." Journal of Neurochemistry. 128 (4), pp. 547-560. https://doi.org/10.1111/jnc.12482
Early Life Stress and Post-Weaning High Fat Diet Alter Tyrosine Hydroxylase Regulation and AT1 Receptor Expression in the Adrenal Gland in a Sex Dependent Manner
Bobrovskaya, Larisa, Maniam, Jayanthi, Ong, Lin Kooi, Dunkley, Peter R. and Morris, Margaret J.. 2013. "Early Life Stress and Post-Weaning High Fat Diet Alter Tyrosine Hydroxylase Regulation and AT1 Receptor Expression in the Adrenal Gland in a Sex Dependent Manner." Neurochemical Research. 38 (4), pp. 826-833. https://doi.org/10.1007/s11064-013-0985-4
Functional Programming of the Autonomic Nervous System by Early Life Immune Exposure: Implications for Anxiety
Sominsky, Luba, Fuller, Erin A., Bondarenko, Evgeny, Ong, Lin Kooi, Averell, Lee, Nalivaiko, Eugene, Dunkley, Peter R., Dickson, Phillip W. and Hodgson, Deborah M.. 2013. "Functional Programming of the Autonomic Nervous System by Early Life Immune Exposure: Implications for Anxiety." PLoS One. 8 (3), pp. 1-13. https://doi.org/10.1371/journal.pone.0057700
Tyrosine Hydroxylase Phosphorylation in Catecholaminergic Brain Regions: A Marker of Activation following Acute Hypotension and Glucoprivation
Damanhuri, Hanafi A., Burke, Peter G. R., Ong, Lin K., Bobrovskaya, Larisa, Dickson, Phillip W., Dunkley, Peter R. and Goodchild, Ann K.. 2012. "Tyrosine Hydroxylase Phosphorylation in Catecholaminergic Brain Regions: A Marker of Activation following Acute Hypotension and Glucoprivation." PLoS One. 7 (11), pp. 1-19. https://doi.org/10.1371/journal.pone.0050535
The Sustained Phase of Tyrosine Hydroxylase Activation In vivo
Ong, Lin Kooi, Sominsky, Luba, Dickson, Phillip W., Hodgson, Deborah M. and Dunkley, Peter R.. 2012. "The Sustained Phase of Tyrosine Hydroxylase Activation In vivo." Neurochemical Research. 37 (9), pp. 1938-1943. https://doi.org/10.1007/s11064-012-0812-3
Increased microglial activation in the rat brain following neonatal exposure to a bacterial mimetic
Sominsky, L., Walker, A. K., Ong, L. K., Tynan, R. J., Walker, F. R. and Hodgson, D. M.. 2012. "Increased microglial activation in the rat brain following neonatal exposure to a bacterial mimetic." Behavioural Brain Research. 226 (1), pp. 351-356. https://doi.org/10.1016/j.bbr.2011.08.038
The effects of footshock and immobilization stress on tyrosine hydroxylase phosphorylation in the rat locus coeruleus and adrenal gland
Ong, L. K., Guan, L., Stutz, B., Dickson, P. W., Dunkley, P. R. and Bobrovskaya, L.. 2011. "The effects of footshock and immobilization stress on tyrosine hydroxylase phosphorylation in the rat locus coeruleus and adrenal gland." Neuroscience. 192, pp. 20-27. https://doi.org/10.1016/j.neuroscience.2011.06.087
Epigenetic Inheritance of Anxiety-Like Behaviour in Rats - Role of Early Life Exposure to a Bacterial Mimetic
Sominsky, L., Walker, A. K., Ong, L., Tynan, R. J., Walker, F. R. and Hodgson, D. M.. 2011. "Epigenetic Inheritance of Anxiety-Like Behaviour in Rats - Role of Early Life Exposure to a Bacterial Mimetic." Journal of Developmental Origins of Health and Disease. 2, pp. S109-S109.
Neonatal respiratory infection and adult re-infection: Effect on glucocorticoid and mineralocorticoid receptors in the hippocampus in BALB/c mice
Wynne, O., Horvat, J. C., Kim, R. Y., Ong, L. K., Smith, R., Hansbro, P. M., Clifton, V. L. and Hodgson, D. M.. 2011. "Neonatal respiratory infection and adult re-infection: Effect on glucocorticoid and mineralocorticoid receptors in the hippocampus in BALB/c mice." Brain, Behavior, and Immunity. 25 (6), pp. 1214-1222. https://doi.org/10.1016/j.bbi.2011.03.014
Sustained Phosphorylation of Tyrosine Hydroxylase at Serine 40 in VIVO
Ong, L. K., Sominsky, L., Walker, A. K., Hodgson, D. M., Goodchild, A. K., Bobrovskaya, L., Dickson, P. W. and Dunkley, P. R.. 2011. "Sustained Phosphorylation of Tyrosine Hydroxylase at Serine 40 in VIVO." 23rd Biennial Meeting of the International Society for Neurochemistry (2011). Athen, Greece 28 Aug - 01 Sep 2011 United Kingdom.
The Effect of Social Defeat on Tyrosine Hydroxylase Phosphorylation in the Rat Brain and Adrenal Gland
Ong, Lin Kooi, Bobrovskaya, Larisa, Walker, Frederick R., Day, Trevor A., Dickson, Phillip W. and Dunkley, Peter R.. 2011. "The Effect of Social Defeat on Tyrosine Hydroxylase Phosphorylation in the Rat Brain and Adrenal Gland." Neurochemical Research. 36 (1), pp. 27-33. https://doi.org/10.1007/s11064-010-0255-7
Tyrosine hydroxylase phosphorylation in response to footshock and restraint stress
Ong, L., Guan, L., Stutz, B., Dickson, P., Dunkley, P. and Bobrovskaya, L.. 2010. "Tyrosine hydroxylase phosphorylation in response to footshock and restraint stress." Journal of Neurochemistry. 115, pp. 77-77.
Signal transduction pathways and tyrosine hydroxylase regulation in the adrenal medulla following glucoprivation: An in vivo analysis
Bobrovskaya, Larisa, Damanhuri, Hanafi A., Ong, Lin Kooi, Schneider, Jennifer J., Dickson, Phillip W., Dunkley, Peter R. and Goodchild, Ann K.. 2010. "Signal transduction pathways and tyrosine hydroxylase regulation in the adrenal medulla following glucoprivation: An in vivo analysis." Neurochemistry International: the journal for the publication of cellular and molecular aspects of neurochemistry. 57 (2), pp. 162-167. https://doi.org/10.1016/j.neuint.2010.05.009
The effect of social conflict on tyrosine hydroxylase phosphorylation in catecholamine-producing cells from sprague-dawley rats
Ong, L., Bobrovskaya, L., Walker, F., Day, Trevor, Dickson, P. and Dunkley, P.. 2009. "The effect of social conflict on tyrosine hydroxylase phosphorylation in catecholamine-producing cells from sprague-dawley rats." 22nd Biennial Meeting of the International Society for Neurochemistry & Asian Pacific Society for Neurochemistry (2009). South Korea 23 - 29 Aug 2009 United Kingdom.
Cross-neutralisation of Australian brown and tiger snake venoms with commercial antivenoms: Cross-reactivity or antivenom mixtures?
O’Leary, Margaret A., Schneider, Jennifer J., Prakash Krishnan, Brian, Lavis, Christopher, McKendry, Amy, Ong, Lin Kooi and Isbister, Geoffrey K.. 2007. "Cross-neutralisation of Australian brown and tiger snake venoms with commercial antivenoms: Cross-reactivity or antivenom mixtures?" Toxicon. 50 (2), pp. 206-213. https://doi.org/10.1016/j.toxicon.2007.03.014