Brain regions showing white matter loss in Huntington's Disease are enriched for synaptic and metabolic genes

Journal article

McColgan, Peter, Gregory, Sarah, Seunarine, Kiran K., Razi, Adeel, Papoutsi, Marina, Johnson, Eileanoir B., Dürr, Alexandra, Roos, Raymund, Leavitt, Blair R., Holmans, Peter, Scahill, Rachael I., Clark, Chris A., Rees, Geraint, Tabrizi, Sarah J., Coleman, A., Decolongon, J., Fan, M., Petkau, T., Jauffret, C., ... Crawfurd, D.. (2018). Brain regions showing white matter loss in Huntington's Disease are enriched for synaptic and metabolic genes. Biological Psychiatry. 83(5), pp. 456-465. https://doi.org/10.1016/j.biopsych.2017.10.019
AuthorsMcColgan, Peter, Gregory, Sarah, Seunarine, Kiran K., Razi, Adeel, Papoutsi, Marina, Johnson, Eileanoir B., Dürr, Alexandra, Roos, Raymund, Leavitt, Blair R., Holmans, Peter, Scahill, Rachael I., Clark, Chris A., Rees, Geraint, Tabrizi, Sarah J., Coleman, A., Decolongon, J., Fan, M., Petkau, T., Jauffret, C., Justo, D., Lehericy, S., Nigaud, K., Valabrègue, R., Schoonderbeek, A., ’t Hart, E. P., Hensman Moss, D. J., Ghosh, R., Crawford, H., Papoutsi, M., Berna, C., Mahaleskshmi, D., Reilmann, R., Weber, N., Labuschagne, I., Stout, J., Landwehrmeyer, B., Orth, M., Mayer, I., Johnson, H. and Crawfurd, D.
Abstract

Background
The earliest white matter changes in Huntington’s disease are seen before disease onset in the premanifest stage around the striatum, within the corpus callosum, and in posterior white matter tracts. While experimental evidence suggests that these changes may be related to abnormal gene transcription, we lack an understanding of the biological processes driving this regional vulnerability.

Methods
Here, we investigate the relationship between regional transcription in the healthy brain, using the Allen Institute for Brain Science transcriptome atlas, and regional white matter connectivity loss at three time points over 24 months in subjects with premanifest Huntington’s disease relative to control participants. The baseline cohort included 72 premanifest Huntington’s disease participants and 85 healthy control participants.

Results
We show that loss of corticostriatal, interhemispheric, and intrahemispheric white matter connections at baseline and over 24 months in premanifest Huntington’s disease is associated with gene expression profiles enriched for synaptic genes and metabolic genes. Corticostriatal gene expression profiles are predominately associated with motor, parietal, and occipital regions, while interhemispheric expression profiles are associated with frontotemporal regions. We also show that genes with known abnormal transcription in human Huntington’s disease and animal models are overrepresented in synaptic gene expression profiles, but not in metabolic gene expression profiles.

Conclusions
These findings suggest a dual mechanism of white matter vulnerability in Huntington’s disease, in which abnormal transcription of synaptic genes and metabolic disturbance not related to transcription may drive white matter loss.

Keywordsconnectome; genetics; Huntington’s Disease; imaging; transcription; white matter
Year2018
JournalBiological Psychiatry
Journal citation83 (5), pp. 456-465
PublisherElsevier Inc.
ISSN0006-3223
Digital Object Identifier (DOI)https://doi.org/10.1016/j.biopsych.2017.10.019
Scopus EID2-s2.0-85034747457
Open accessPublished as ‘gold’ (paid) open access
Page range456-465
FunderWellcome Trust
National Institute for Health Research (NIHR)
University College London Hospitals (UCLH)
Biomedical Research Centre (BRC), National Institute for Health Research
Publisher's version
License
File Access Level
Open
Output statusPublished
Publication dates
Online26 Oct 2017
Publication process dates
Accepted07 Oct 2017
Deposited24 Nov 2022
Grant ID091593/Z/10/Z
103437/Z/13/Z
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The cognitive burden in Huntington's disease: Pathology, phenotype and mechanisms of compensation
Papoutsi, Marina, Labuschagne, Izelle, Tabrizi, Sarah J. and Stout, Julie C.. (2014). The cognitive burden in Huntington's disease: Pathology, phenotype and mechanisms of compensation. Movement Disorders Society. 29(5), pp. 673 - 683. https://doi.org/10.1002/mds.25864
A comparison of executive function in Body Dysmorphic Disorder (BDD) and Obsessive-Compulsive Disorder (OCD)
Labuschagne, Izelle, Rossell, Susan, Dunai, Judith, Castle, David and Kyrios, Michael. (2013). A comparison of executive function in Body Dysmorphic Disorder (BDD) and Obsessive-Compulsive Disorder (OCD). Journal of Obsessive-Compulsive and Related Disorders. 2(3), pp. 257 - 262. https://doi.org/10.1016/j.jocrd.2013.05.003
Oxytocin enhances resting-state connectivity between amygdala and medial frontal cortex
Sripada, Chandra, Phan, Kinhluan, Labuschagne, Izelle, Welsh, Robert, Nathan, Pradeep and Wood, Amanda. (2013). Oxytocin enhances resting-state connectivity between amygdala and medial frontal cortex. International Journal of Neuropsychopharmacology (print). 16(2), pp. 255 - 260. https://doi.org/10.1017/S1461145712000533
Emotional face recognition deficits and medication effects in pre-manifest through stage-II Huntington's disease
Labuschagne, Izelle, Jones, Rebecca, Callaghan, Jenny, Whitehead, Daisy, Dumas, Eve, Say, Miranda, Hart, Ellen, Justo, Damian, Coleman, Allison, Dar Santos, Rachelle, Frost, Chris, Craufurd, David, Trabrizi, Sarah and Stout, Julie. (2013). Emotional face recognition deficits and medication effects in pre-manifest through stage-II Huntington's disease. Psychiatry Research. 207(1-2), pp. 118 - 126. https://doi.org/10.1016/j.psychres.2012.09.022
Emotional face recognition deficits and medication effects in pre-manifest through stage-II Huntington's disease
Labuschagne, Izelle, Jones, Rebecca, Callaghan, Jenny, Whitehead, Daisy, Dumas, Eve, Say, Miranda, Hart, Ellen, Justo, Damian, Coleman, Allison, Dar Santos, Rachelle, Frost, Chris, Craufurd, David, Tabrizi, Sarah and Stout, Julie. (2013). Emotional face recognition deficits and medication effects in pre-manifest through stage-II Huntington's disease. Psychiatry Research. 207(1-2), pp. 118 - 126. https://doi.org/10.1016/j.psychres.2012.09.022
Oxytocin enhances resting-state connectivity between amygdala and medial frontal cortex
Sripada, Chandra, Phan, Kinhluan, Labuschagne, Izelle, Welsh, Robert, Nathan, Pradeep and Wood, Amanda. (2013). Oxytocin enhances resting-state connectivity between amygdala and medial frontal cortex. International Journal of Neuropsychopharmacology. 16(2), pp. 255 - 260. https://doi.org/10.1017/S1461145712000533
Visual working memory impairment in premanifest gene-carriers and early Huntington's Disease
Dumas, Eve M., Say, Miranda Julia, Jones, Rebecca D., Labuschagne, Izelle, O'Regan, Alison M., Hart, Ellen P., van den Bogaard, Simon J. A., Queller, Sarah, Justo, Damian, Coleman, Allison J., dar Santos, Rachelle C., Durr, Alexandra, Leavitt, Blair R., Tabrizi, Sarah J., Roos, Raymund A. C. and Stout, Julie C.. (2012). Visual working memory impairment in premanifest gene-carriers and early Huntington's Disease. Journal of Huntington's Disease. 1(1), pp. 97 - 106. https://doi.org/10.3233/JHD-2012-120010
Evaluation of longitudinal 12 and 24 month cognitive outcomes in premanifest and early Huntington's disease
Stout, Julie, Jones, Rebecca, Labuschagne, Izelle, O'Regan, Alison, Say, Miranda, Dumas, Eve, Queller, Sarah, Justo, Damian, Dar Santos, Rachelle, Coleman, Allison, Hart, Ellen, Durr, Alexandra, Leavitt, Blair, Roos, Raymund, Langbehn, Doug, Tabrizi, Sarah J. and Frost, Chris. (2012). Evaluation of longitudinal 12 and 24 month cognitive outcomes in premanifest and early Huntington's disease. Journal of Neurology, Neurosurgery and Psychiatry. 83(7), pp. 687 - 694. https://doi.org/10.1136/jnnp-2011-301940
Medial frontal hyperactivity to sad faces in generalized social anxiety disorder and modulation by oxytocin
Labuschagne, Izelle, Phan, K. Luan, Wood, Amanda, Angstadt, Mike, Chua, Phyllis, Heinrichs, Markus, Stout, Julie C., Nathan, Pradeep J. and Pradeep,. (2012). Medial frontal hyperactivity to sad faces in generalized social anxiety disorder and modulation by oxytocin. International Journal of Neuropsychopharmacology (print). 15(7), pp. 883 - 896. https://doi.org/10.1017/S1461145711001489
Evaluation of longitudinal 12 and 24 month cognitive outcomes in premanifest and early Huntington's disease
Stout, Julie, Jones, Rebecca, Labuschagne, Izelle, O'Regan, Alison, Say, Miranda, Dumas, Eve, Queller, Sarah, Justo, Damian, Dar Santos, Rachelle, Coleman, Allison, Hart, Ellen, Durr, Alexandra, Leavitt, Blair, Roos, Raymund, Langbehn, Douglas, Tabrizi, Sarah J. and Frost, Chris. (2012). Evaluation of longitudinal 12 and 24 month cognitive outcomes in premanifest and early Huntington's disease. Journal of Neurology, Neurosurgery and Psychiatry. 83(7), pp. 687 - 694. https://doi.org/10.1136/jnnp-2011-301940
What the cognitive deficits in body dysmorphic disorder tell us about the underlying neurobiology: An investigation of three cases
Labuschagne, Izelle, Castle, David and Rossell, Susan L.. (2011). What the cognitive deficits in body dysmorphic disorder tell us about the underlying neurobiology: An investigation of three cases. International Journal of Cognitive Therapy. 4(1), pp. 21 - 33. https://doi.org/10.1521/ijct.2011.4.1.21
Oxytocin attenuates amygdala reactivity to fear in generalized social anxiety disorder
Labuschagne, Izelle, Phan, K. Luan, Wood, Amanda G., Angstadt, Mike, Chua, Phyllis, Heinrichs, Markus, Stout, Julie C. and Nathan, Pradeep. (2010). Oxytocin attenuates amygdala reactivity to fear in generalized social anxiety disorder. Neuropsychopharmacology. 35(12), pp. 2403 - 2413. https://doi.org/10.1038/npp.2010.123
Augmenting serotonin neurotransmission with citalopram modulates emotional expression decoding but not structural encoding of moderate intensity sad facial emotional stimuli: An event-related potential (ERP) investigation
Labuschagne, Izelle, Croft, Rodney, Phan, K. Luan and Nathan, Pradeep. (2010). Augmenting serotonin neurotransmission with citalopram modulates emotional expression decoding but not structural encoding of moderate intensity sad facial emotional stimuli: An event-related potential (ERP) investigation. Journal of Psychopharmacology. 24(8), pp. 1153 - 1164. https://doi.org/10.1177/0269881108097878
Executive function in body dysmorphic disorder
Dunai, Judith, Labuschagne, Izelle, Castle, David J., Kyrios, Michael and Rossell, Susan. (2010). Executive function in body dysmorphic disorder. Psychological Medicine. 40(9), pp. 1541 - 1548. https://doi.org/10.1017/S003329170999198X
An examination of delusional thinking and cognitive styles in body dysmorphic disorder
Labuschagne, Izelle, Castle, David J., Dunai, Judith, Kyrios, Michael and Rossell, Susan. (2010). An examination of delusional thinking and cognitive styles in body dysmorphic disorder. Australian and New Zealand Journal of Psychiatry. 44(8), pp. 706 - 712. https://doi.org/10.3109/00048671003671007
Evidence for modulation of facial emotional processing bias during emotional expression decoding by serotonergic and noradrenergic antidepressants: An event-related potential (ERP) study
Kerestes, Rebecca, Labuschagne, Izelle, Croft, Rodney, O'Neill, Barry, Bhagwagar, Zubin M., Phan, K Luan and Nathan, Pradeep. (2009). Evidence for modulation of facial emotional processing bias during emotional expression decoding by serotonergic and noradrenergic antidepressants: An event-related potential (ERP) study. Psychopharmacology. 202(4), pp. 621 - 634. https://doi.org/10.1007/s00213-008-1340-3