Mass Spectrometry Imaging of Biomarker Lipids for Phagocytosis and Signalling During Focal Cerebral Ischaemia

Overview

Journal Sci Rep

Specialty Science

Date 2016 Dec 23

PMID 28004822

Citations 42

Authors

Mette M B Nielsen

Kate L Lambertsen

Bettina H Clausen

Morten Meyer

Dhaka R Bhandari

Soren T Larsen

Steen S Poulsen

Bernhard Spengler

Christian Janfelt

Harald S Hansen

Affiliations

Soon will be listed here.

Abstract

Focal cerebral ischaemia has an initial phase of inflammation and tissue injury followed by a later phase of resolution and repair. Mass spectrometry imaging (desorption electrospray ionization and matrix assisted laser desorption ionization) was applied on brain sections from mice 2 h, 24 h, 5d, 7d, and 20d after permanent focal cerebral ischaemia. Within 24 h, N-acyl-phosphatidylethanolamines, lysophosphatidylcholine, and ceramide accumulated, while sphingomyelin disappeared. At the later resolution stages, bis(monoacylglycero)phosphate (BMP(22:6/22:6)), 2-arachidonoyl-glycerol, ceramide-phosphate, sphingosine-1-phosphate, lysophosphatidylserine, and cholesteryl ester appeared. At day 5 to 7, dihydroxy derivates of docosahexaenoic and docosapentaenoic acid, some of which may be pro-resolving mediators, e.g. resolvins, were found in the injured area, and BMP(22:6/22:6) co-localized with the macrophage biomarker CD11b, and probably with cholesteryl ester. Mass spectrometry imaging can visualize spatiotemporal changes in the lipidome during the progression and resolution of focal cerebral inflammation and suggests that BMP(22:6/22:6) and N-acyl-phosphatidylethanolamines can be used as biomarkers for phagocytizing macrophages/microglia cells and dead neurones, respectively.

Citing Articles

Accumulation of Bioactive Lipid Species in LPS-Induced Neuroinflammation Models Analysed with Multi-Modal Mass Spectrometry Imaging.

Razo I, Shea K, Allen T, Boutin H, McMahon A, Lockyer N Int J Mol Sci. 2024; 25(22).

PMID: 39596102 PMC: 11594259. DOI: 10.3390/ijms252212032.

Glycolipidomics of Liver Flukes and Host Tissues during Fascioliasis: Insights from Mass Spectrometry Imaging.

Luh D, Ghezellou P, Heiles S, Gramberg S, Haeberlein S, Spengler B ACS Infect Dis. 2024; 10(12):4233-4245.

PMID: 39510517 PMC: 11650768. DOI: 10.1021/acsinfecdis.4c00551.

Dynamic Brain Lipid Profiles Modulate Microglial Lipid Droplet Accumulation and Inflammation Under Ischemic Conditions in Mice.

Wei W, Lattau S, Xin W, Pan Y, Tatenhorst L, Zhang L Adv Sci (Weinh). 2024; 11(41):e2306863.

PMID: 39252446 PMC: 11538718. DOI: 10.1002/advs.202306863.

Sphingolipid changes in mouse brain and plasma after mild traumatic brain injury at the acute phases.

Mondal K, Del Mar N, Gary A, Grambergs R, Yousuf M, Tahia F Lipids Health Dis. 2024; 23(1):200.

PMID: 38937745 PMC: 11209960. DOI: 10.1186/s12944-024-02186-x.

Metabolomic discoveries for early diagnosis and traditional Chinese medicine efficacy in ischemic stroke.

Wei L, Chen S, Deng X, Liu Y, Wang H, Gao X Biomark Res. 2024; 12(1):63.

PMID: 38902829 PMC: 11188286. DOI: 10.1186/s40364-024-00608-7.

References

Hansen H, Schmid P, Bittigau P, Lastres-Becker I, Berrendero F, Manzanares J . Anandamide, but not 2-arachidonoylglycerol, accumulates during in vivo neurodegeneration. J Neurochem. 2001; 78(6):1415-27. DOI: 10.1046/j.1471-4159.2001.00542.x. View

Degn M, Lambertsen K, Petersen G, Meldgaard M, Artmann A, Clausen B . Changes in brain levels of N-acylethanolamines and 2-arachidonoylglycerol in focal cerebral ischemia in mice. J Neurochem. 2007; 103(5):1907-16. DOI: 10.1111/j.1471-4159.2007.04892.x. View

Mechoulam R, Parker L . The endocannabinoid system and the brain. Annu Rev Psychol. 2012; 64:21-47. DOI: 10.1146/annurev-psych-113011-143739. View

Bouschen W, Schulz O, Eikel D, Spengler B . Matrix vapor deposition/recrystallization and dedicated spray preparation for high-resolution scanning microprobe matrix-assisted laser desorption/ionization imaging mass spectrometry (SMALDI-MS) of tissue and single cells. Rapid Commun Mass Spectrom. 2010; 24(3):355-64. DOI: 10.1002/rcm.4401. View

Robichaud G, Garrard K, Barry J, Muddiman D . MSiReader: an open-source interface to view and analyze high resolving power MS imaging files on Matlab platform. J Am Soc Mass Spectrom. 2013; 24(5):718-21. PMC: 3693088. DOI: 10.1007/s13361-013-0607-z. View

Panikashvili D, Simeonidou C, Hanus L, Breuer A, Mechoulam R, Shohami E . An endogenous cannabinoid (2-AG) is neuroprotective after brain injury. Nature. 2001; 413(6855):527-31. DOI: 10.1038/35097089. View

Hankin J, Farias S, Barkley R, Heidenreich K, Frey L, Hamazaki K . MALDI mass spectrometric imaging of lipids in rat brain injury models. J Am Soc Mass Spectrom. 2011; 22(6):1014-21. PMC: 4537074. DOI: 10.1007/s13361-011-0122-z. View

Hansen H, Lauritzen L, Strand A, Vinggaard A, Frandsen A, Schousboe A . Characterization of glutamate-induced formation of N-acylphosphatidylethanolamine and N-acylethanolamine in cultured neocortical neurons. J Neurochem. 1997; 69(2):753-61. DOI: 10.1046/j.1471-4159.1997.69020753.x. View

Shohami E, Cohen-Yeshurun A, Magid L, Algali M, Mechoulam R . Endocannabinoids and traumatic brain injury. Br J Pharmacol. 2011; 163(7):1402-10. PMC: 3165950. DOI: 10.1111/j.1476-5381.2011.01343.x. View

10.

Goto-Inoue N, Hayasaka T, Zaima N, Setou M . Imaging mass spectrometry for lipidomics. Biochim Biophys Acta. 2011; 1811(11):961-9. DOI: 10.1016/j.bbalip.2011.03.004. View

11.

Wellner N, Diep T, Janfelt C, Hansen H . N-acylation of phosphatidylethanolamine and its biological functions in mammals. Biochim Biophys Acta. 2012; 1831(3):652-62. DOI: 10.1016/j.bbalip.2012.08.019. View

12.

Roux A, Muller L, Jackson S, Post J, Baldwin K, Hoffer B . Mass spectrometry imaging of rat brain lipid profile changes over time following traumatic brain injury. J Neurosci Methods. 2016; 272:19-32. PMC: 7577232. DOI: 10.1016/j.jneumeth.2016.02.004. View

13.

Hattori K, Kajimura M, Hishiki T, Nakanishi T, Kubo A, Nagahata Y . Paradoxical ATP elevation in ischemic penumbra revealed by quantitative imaging mass spectrometry. Antioxid Redox Signal. 2010; 13(8):1157-67. PMC: 2956403. DOI: 10.1089/ars.2010.3290. View

14.

Hansen H, Ikonomidou C, Bittigau P, Hansen S, Hansen H . Accumulation of the anandamide precursor and other N-acylethanolamine phospholipids in infant rat models of in vivo necrotic and apoptotic neuronal death. J Neurochem. 2001; 76(1):39-46. DOI: 10.1046/j.1471-4159.2001.00006.x. View

15.

Girod M, Shi Y, Cheng J, Cooks R . Mapping lipid alterations in traumatically injured rat spinal cord by desorption electrospray ionization imaging mass spectrometry. Anal Chem. 2010; 83(1):207-15. PMC: 3013616. DOI: 10.1021/ac102264z. View

16.

Hanrieder J, Phan N, Kurczy M, Ewing A . Imaging mass spectrometry in neuroscience. ACS Chem Neurosci. 2013; 4(5):666-79. PMC: 3656743. DOI: 10.1021/cn400053c. View

17.

Serhan C . Pro-resolving lipid mediators are leads for resolution physiology. Nature. 2014; 510(7503):92-101. PMC: 4263681. DOI: 10.1038/nature13479. View

18.

Nomura D, Morrison B, Blankman J, Long J, Kinsey S, Marcondes M . Endocannabinoid hydrolysis generates brain prostaglandins that promote neuroinflammation. Science. 2011; 334(6057):809-13. PMC: 3249428. DOI: 10.1126/science.1209200. View

19.

Galvani S, Sanson M, Blaho V, Swendeman S, Obinata H, Conger H . HDL-bound sphingosine 1-phosphate acts as a biased agonist for the endothelial cell receptor S1P1 to limit vascular inflammation. Sci Signal. 2015; 8(389):ra79. PMC: 4768813. DOI: 10.1126/scisignal.aaa2581. View

20.

Hansen H, Hansen S, Schousboe A, Hansen H . Determination of the phospholipid precursor of anandamide and other N-acylethanolamine phospholipids before and after sodium azide-induced toxicity in cultured neocortical neurons. J Neurochem. 2000; 75(2):861-71. DOI: 10.1046/j.1471-4159.2000.0750861.x. View