X-ray fluorescence mapping of brain tissue reveals the profound extent of trace element dysregulation in stroke pathophysiology

被引:1
作者
Pushie, M. Jake [1 ]
Sylvain, Nicole J. [1 ]
Hou, Huishu [1 ]
Pendleton, Nicole [1 ]
Wang, Richard [2 ]
Zimmermann, Liam [2 ]
Pally, Maxwell [3 ]
Cayabyab, Francisco S. [1 ]
Peeling, Lissa [1 ]
Kelly, Michael E. [1 ]
机构
[1] Univ Saskatchewan, Coll Med, Dept Surg, Div Neurosurg, Saskatoon, SK S7N 5E5, Canada
[2] Univ Saskatchewan, Coll Med, Dept Med, Saskatoon, SK S7N 5E5, Canada
[3] Univ Saskatchewan, Coll Arts & Sci Anat Physiol & Pharmacol, Saskatoon, SK S7N 5E5, Canada
基金
美国国家卫生研究院; 加拿大健康研究院; 加拿大自然科学与工程研究理事会; 加拿大创新基金会;
关键词
X-ray fluorescence microscopy; brain metals; trace element imaging; ischaemia; stroke; NUTRITIONAL IMMUNITY; COPPER; IRON; PH; INFLAMMATION; RELEASE; BINDING; METALS;
D O I
10.1093/mtomcs/mfae054
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
The brain is a privileged organ with regard to its trace element composition and maintains a robust barrier system to sequester this specialized environment from the rest of the body and the vascular system. Stroke is caused by loss of adequate blood flow to a region of the brain. Without adequate blood flow ischaemic changes begin almost immediately, triggering an ischaemic cascade, characterized by ion dysregulation, loss of function, oxidative damage, cellular degradation, and breakdown of the barrier that helps maintain this environment. Ion dysregulation is a hallmark of stroke pathophysiology and we observe that most elements in the brain are dysregulated after stroke. X-ray fluorescence-based detection of physiological changes in the neurometallome after stroke reveals profound ion dysregulation within the lesion and surrounding tissue. Not only are most elements significantly dysregulated after stroke, but the level of dysregulation cannot be predicted from a cell-level description of dysregulation. X-ray fluorescence imaging reveals that the stroke lesion retains <25% of essential K+ after stroke, but this element is not concomitantly elevated elsewhere in the organ. Moreover, elements like Na+, Ca2+, and Cl- are vastly elevated above levels available in normal brain tissue (>400%, >200%, and >150%, respectively). We hypothesize that weakening of the blood-brain barrier after stroke allows elements to freely diffuse down their concentration gradient so that the stroke lesion is in equilibrium with blood (and the compartments containing brain interstitial fluid and cerebrospinal fluid). The change observed for the neurometallome likely has consequences for the potential to rescue infarcted tissue, but also presents specific targets for treatment.
引用
收藏
页数:14
相关论文
共 79 条
[1]   Epidemiology, Risk Factors, and Clinical Features of Intracerebral Hemorrhage: An Update [J].
An, Sang Joon ;
Kim, Tae Jung ;
Yoon, Byung-Woo .
JOURNAL OF STROKE, 2017, 19 (01) :3-10
[2]  
Back T, 2000, ANN NEUROL, V47, P485, DOI 10.1002/1531-8249(200004)47:4<485::AID-ANA12>3.0.CO
[3]  
2-8
[4]   Revisiting cerebral postischemic reperfusion injury: new insights in understanding reperfusion failure, hemorrhage, and edema [J].
Bai, Jilin ;
Lyden, Patrick D. .
INTERNATIONAL JOURNAL OF STROKE, 2015, 10 (02) :143-152
[5]   Imaging of metals in biological tissue by laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS): state of the art and future developments [J].
Becker, J. .
JOURNAL OF MASS SPECTROMETRY, 2013, 48 (02) :255-268
[6]   Bioimaging mass spectrometry of trace elements - recent advance and applications of LA-ICP-MS: A review [J].
Becker, J. Sabine ;
Matusch, Andreas ;
Wu, Bei .
ANALYTICA CHIMICA ACTA, 2014, 835 :1-18
[7]   Immune Cell Infiltration into the Brain After Ischemic Stroke in Humans Compared to Mice and Rats: a Systematic Review and Meta-Analysis [J].
Beuker, Carolin ;
Strecker, Jan-Kolja ;
Rawal, Rajesh ;
Schmidt-Pogoda, Antje ;
Ruck, Tobias ;
Wiendl, Heinz ;
Klotz, Luisa ;
Schaebitz, Wolf-Ruediger ;
Sommer, Clemens J. ;
Minnerup, Heike ;
Meuth, Sven G. ;
Minnerup, Jens .
TRANSLATIONAL STROKE RESEARCH, 2021, 12 (06) :976-990
[8]   Zinc: The Brain's Dark Horse [J].
Bitanihirwe, Byron K. Y. ;
Cunningham, Miles G. .
SYNAPSE, 2009, 63 (11) :1029-1049
[9]   A comparison of sample preparation strategies for biological tissues and subsequent trace element analysis using LA-ICP-MS [J].
Bonta, Maximilian ;
Torok, Szilvia ;
Hegedus, Balazs ;
Dome, Balazs ;
Limbeck, Andreas .
ANALYTICAL AND BIOANALYTICAL CHEMISTRY, 2017, 409 (07) :1805-1814
[10]   A review of concepts and methods for FTIR imaging of biomarker changes in the post-stroke brain [J].
Boseley, Rhiannon E. ;
Sylvain, Nicole J. ;
Peeling, Lissa ;
Kelly, Michael E. ;
Pushie, M. Jake .
BIOCHIMICA ET BIOPHYSICA ACTA-BIOMEMBRANES, 2024, 1866 (03)