Citation: Chao Zhao, Chenyu Gao, Zhiyi Yang, Tianyou Cao, Qian Luo, Zhijun Zhang. Whole brain lipid dyshomeostasis in depressive-like behavior young adult rats: Mapping by mass spectrometry imaging-based spatial omics[J]. Chinese Chemical Letters, ;2025, 36(10): 111089. doi: 10.1016/j.cclet.2025.111089 shu

Whole brain lipid dyshomeostasis in depressive-like behavior young adult rats: Mapping by mass spectrometry imaging-based spatial omics

Chao Zhao ^{a, b, c, *,} ,
Chenyu Gao ^{a, b, 1} ,
Zhiyi Yang ^c ,
Tianyou Cao ^c ,
Qian Luo ^{c, d, *,} ,
Zhijun Zhang ^{a, b, *,}

a.
Department of Neurology in Affiliated Zhongda Hospital and Jiangsu Provincial Medical Key Discipline, School of Medicine, Institute of Neuropsychiatry, Key Laboratory of Developmental Genes and Human Disease, Southeast University, Nanjing 210009, China
b.
Shenzhen Key Laboratory of Precision Diagnosis and Treatment of Depression, Department of Mental Health and Public Health, Faculty of Life and Health Sciences of Shenzhen University of Advanced Technology, The Brain Cognition and Brain Disease Institute to Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China
c.
Institute of Scientific Instrumentation, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China
d.
University of Chinese Academy of Sciences, Beijing 100006, China

chao.zhao@siat.ac.cn

qian.luo@siat.ac.cn

janemengzhang@vip.163.com

Received Date: 2 October 2024
Revised Date: 4 February 2025
Accepted Date: 13 March 2025
Available Online: 14 March 2025

Figures(4)

There is growing evidence that lipid metabolism instability in depressive disorder may be a core early pathological event associated with numerous pathogenesis hypotheses. However, spatial distributions and quantitative changes of lipids in specific brain regions associated with depressive disorder are far from elucidated. In the present study, lipid profiling characteristics of whole brain sections are systematically determined by using matrix-assisted laser desorption ionization-mass spectrometry imaging (MALDI-MSI)-combined with histomorphological analysis in rats with depressive-like behavior induced by multiple early life stress (mELS) and unstressed control. Lipid dyshomeostasis and different degrees of metabolic disturbance occur in the eight paired representative brain sections from micro-region and molecular level. More specifically, 17 lipid molecules show the severe dyshomeostasis between inter-group (control and depressed rats) or intra-group (multiple emotion-regulation-related brain regions). Quite specially, phosphatidylcholine (PC) (39:6) expression in section 7 is significantly upregulated only in the amygdala of depressed rat relative to control rat, by contrast, up-regulated phosphatidylglycerol (PG) (34:2) in section 2 emerges in the medial prefrontal cortex, insular cortex, and nucleus accumbens simultaneously. Linking spatial distribution to quantitative variation of lipids from the whole brain sections contributes the uncovering of new insights in causal mechanism of lipid dyshomeostasis in depression investigation and related targeting interventions.
- Depressive disorder,
- Lipid dyshomeostasis,
- Mass spectrometry imaging,
- Spatial omics,
- Whole brain imaging,
- Adolescent depression
1. [1]
  G.S. Malhi, J.J. Mann, Lancet 392 (2018) 2299–2312. doi: 10.1016/S0140-6736(18)31948-2
2. [2]
  A. Thapar, O. Eyre, V. Patel, et al., Lancet 400 (2022) 617–631. doi: 10.1016/S0140-6736(22)01012-1
3. [3]
  M.M. Barker, B. Beresford, M. Bland, et al., JAMA Pediatr. 173 (2019) 835–844. doi: 10.1001/jamapediatrics.2019.1712
4. [4]
  M.A. Forti-Buratti, R. Saikia, E.L. Wilkinson, et al., Eur. Child Adoles. Psy. 25 (2016) 1045–1054. doi: 10.1007/s00787-016-0834-5
5. [5]
  C.P. Muller, M. Reichel, C. Muhle, et al., Biochim. Biophys. Acta 1851 (2015) 1052–1065. doi: 10.1016/j.bbalip.2014.12.014
6. [6]
  E.A. Lucassen, G. Cizza, Curr. Obes. Rep. 1 (2012) 208–215. doi: 10.1007/s13679-012-0028-5
7. [7]
  P.R. Angelova, N. Esteras, A.Y. Abramov, Med. Res. Rev. 41 (2021) 770–784. doi: 10.1002/med.21712
8. [8]
  M. Maes, P. Galecki, Y.S. Chang, et al., Prog. Neuro-Psychoph. 35 (2011) 676–692. doi: 10.1016/j.pnpbp.2010.05.004
9. [9]
  L. Cui, S. Li, S. Wang, et al., Signal Transduct. Target Ther. 9 (2024) 30. doi: 10.1038/s41392-024-01738-y
10. [10]
  E. Gulbins, M. Palmada, M. Reichel, et al., Nat. Med. 19 (2013) 934–938. doi: 10.1038/nm.3214
11. [11]
  A. Gulbins, F. Schumacher, K.A. Becker, et al., Mol. Psychiatr. 23 (2018) 2324–2346. doi: 10.1038/s41380-018-0090-9
12. [12]
  J.H. Yoon, Y. Seo, Y.S. Jo, et al., Sci. Adv. 8 (2022) eadc9317. doi: 10.1126/sciadv.adc9317
13. [13]
  C. Zhao, L. Guo, J.Y. Dong, et al., Innovation 2 (2021) 100151.
14. [14]
  Q. Zhang, Y. Li, P. Sui, et al., Talanta 266 (2024) 125022. doi: 10.1016/j.talanta.2023.125022
15. [15]
  J. Matsumoto, Y. Sugiura, D. Yuki, et al., Anal. Bioanal. Chem. 400 (2011) 1933–1943. doi: 10.1007/s00216-011-4909-3
16. [16]
  D.L. Van den Hove, G. Kenis, A. Brass, et al., Eur. Neuropsychopharm. 23 (2013) 1226–1246. doi: 10.1016/j.euroneuro.2012.09.011
17. [17]
  S. Boku, H. Toda, S. Nakagawa, et al., Biol. Psychiat. 77 (2015) 335–344. doi: 10.1016/j.biopsych.2014.07.008
18. [18]
  Y. Zhang, Y. Wang, H. Lei, et al., BMC Psychiatry 17 (2017) 171. doi: 10.1186/s12888-017-1335-x
19. [19]
  P. Sengupta, Int. J. Prevent. Med. 4 (2013) 624–630.
20. [20]
  G.A. Johnson, E. Calabrese, A. Badea, et al., NeuroImage. 62 (2012) 1848-1856. doi: 10.1016/j.neuroimage.2012.05.041
21. [21]
  Z.W. Ma, P. Perez, Z.L. Ma, et al., NeuroImage. 170 (2018) 95-112. doi: 10.1016/j.neuroimage.2016.07.007
22. [22]
  G.A. Johnson, R. Laoprasert, R.J. Anderson, et al., NeuroImage. 242 (2021) 118470. doi: 10.1016/j.neuroimage.2021.118470
23. [23]
  M. Malezieux, A.S. Klein, N. Gogolla, Annu. Rev. Neurosci. 46 (2023) 211–231. doi: 10.1146/annurev-neuro-111020-103314
24. [24]
  A. Walther, C.V. Cannistraci, K. Simons, et al., Front. Psychiatry 9 (2018) 459.
25. [25]
  E.L. Riddle, K.S. Rau, M.K. Topham, et al., Eur. J. Pharmacol. 458 (2003) 31–36. doi: 10.1016/S0014-2999(02)02727-9
26. [26]
  S. Akiyama, H. Nagai, S. Oike, et al., Sci. Rep. 12 (2022) 11385. doi: 10.1038/s41598-022-15461-7
27. [27]
  Y. He, Y. Wang, Z. Wu, et al., Metab. Brain Dis. 35 (2020) 649–659. doi: 10.1007/s11011-020-00557-8
28. [28]
  P. Zheng, J. Wu, H. Zhang, et al., Mol. Psychiatr. 26 (2021) 2380–2392. doi: 10.1038/s41380-020-0744-2
29. [29]
  X. Wu, H. Xu, N. Zeng, et al., CNS Neurosci. Ther. 30 (2024) e14455. doi: 10.1111/cns.14455
30. [30]
  F.G. Ibáñez, T. Halvorson, K. Sharma, et al., Brain Behav. Immun. 114 (2023) 383–406. doi: 10.1016/j.bbi.2023.09.006
31. [31]
  S.S. Xue, C.H. Zhou, F. Xue, et al., Prog. Neuro-Psychoph. 102 (2020) 109946. doi: 10.1016/j.pnpbp.2020.109946
32. [32]
  Y. Song, F. Xiao, J. Aa, et al., Metabolites 14 (2024) 284. doi: 10.3390/metabo14050284
1. [1]
  Yu-Qi Cao , Ying-Jie Lu , Li Zhang , Jing Zhang , Yin-Long Guo . Vacuum promoted on-tissue derivatization strategy: Unravelling spatial distribution of glycerides on tissue. Chinese Chemical Letters, 2024, 35(12): 109788-. doi: 10.1016/j.cclet.2024.109788
2. [2]
  Shuai Guo , Kening Li , Bin Li . Parallel on-tissue chemical derivatization for enhanced molecular annotation of spatial carbonyl submetabolome. Chinese Chemical Letters, 2025, 36(6): 110366-. doi: 10.1016/j.cclet.2024.110366
3. [3]
  Jing Chen , Peisi Xie , Pengfei Wu , Yu He , Zian Lin , Zongwei Cai . MALDI coupled with laser-postionization and trapped ion mobility spectrometry contribute to the enhanced detection of lipids in cancer cell spheroids. Chinese Chemical Letters, 2024, 35(4): 108895-. doi: 10.1016/j.cclet.2023.108895
4. [4]
  Peisi Xie , Jing Chen , Yongjun Xia , Zongwei Cai . MALDI and MALDI-2 mass spectrometry imaging contribute to revealing the alternations in lipid metabolism in germinating soybean seeds. Chinese Chemical Letters, 2025, 36(8): 110595-. doi: 10.1016/j.cclet.2024.110595
5. [5]
  Yanhua Chen , Xian Ding , Jun Zhou , Zhaoying Wang , Yunhai Bo , Ying Hu , Qingce Zang , Jing Xu , Ruiping Zhang , Jiuming He , Fen Yang , Zeper Abliz . Plasma metabolomics combined with mass spectrometry imaging reveals crosstalk between tumor and plasma in gastric cancer genesis and metastasis. Chinese Chemical Letters, 2025, 36(1): 110351-. doi: 10.1016/j.cclet.2024.110351
6. [6]
  Huamei Zhang , Jingjing Liu , Mingyue Li , Shida Ma , Xucong Zhou , Aixia Meng , Weina Han , Jin Zhou . Imaging polarity changes in pneumonia and lung cancer using a lipid droplet-targeted near-infrared fluorescent probe. Chinese Chemical Letters, 2024, 35(12): 110020-. doi: 10.1016/j.cclet.2024.110020
7. [7]
  Zhoupeng Zheng , Shengyi Gong , Qianhua Li , Shiya Zhang , Guoqiang Feng . Lipid droplets and gallbladder targeted fluorescence probe for ratiometric NO imaging in gallstones disease models. Chinese Chemical Letters, 2025, 36(5): 110191-. doi: 10.1016/j.cclet.2024.110191
8. [8]
  Han-Min Wang , Yan-Chen Li , Lu-Lu Sun , Ming-Ye Tang , Jia Liu , Jiahao Cai , Lei Dong , Jia Li , Yi Zang , Hai-Hao Han , Xiao-Peng He . Protein-encapsulated long-wavelength fluorescent probe hybrid for imaging lipid droplets in living cells and mice with non-alcoholic fatty liver. Chinese Chemical Letters, 2024, 35(11): 109603-. doi: 10.1016/j.cclet.2024.109603
9. [9]
  Tian Feng , Yun-Ling Gao , Di Hu , Ke-Yu Yuan , Shu-Yi Gu , Yao-Hua Gu , Si-Yu Yu , Jun Xiong , Yu-Qi Feng , Jie Wang , Bi-Feng Yuan . Chronic sleep deprivation induces alterations in DNA and RNA modifications by liquid chromatography-mass spectrometry analysis. Chinese Chemical Letters, 2024, 35(8): 109259-. doi: 10.1016/j.cclet.2023.109259
10. [10]
  Cheng Guo , Xiaoxiao Zhang , Xiujuan Hong , Yiqiu Hu , Lingna Mao , Kezhi Jiang . Graphene as adsorbent for highly efficient extraction of modified nucleosides in urine prior to liquid chromatography-tandem mass spectrometry analysis. Chinese Chemical Letters, 2024, 35(4): 108867-. doi: 10.1016/j.cclet.2023.108867
11. [11]
  Junmeng Luo , Qiongqiong Wan , Suming Chen . Chemistry-driven mass spectrometry for structural lipidomics at the C=C bond isomer level. Chinese Chemical Letters, 2025, 36(1): 109836-. doi: 10.1016/j.cclet.2024.109836
12. [12]
  Lu Huang , Jiang Wang , Hong Jiang , Lanfang Chen , Huanwen Chen . On-line determination of selenium compounds in tea infusion by extractive electrospray ionization mass spectrometry combined with a heating reaction device. Chinese Chemical Letters, 2025, 36(1): 109896-. doi: 10.1016/j.cclet.2024.109896
13. [13]
  Haiyan Lu , Jiayue Ye , Yiping Wei , Hua Zhang , Konstantin Chingin , Vladimir Frankevich , Huanwen Chen . Tracing molecular margins of lung cancer by internal extractive electrospray ionization mass spectrometry. Chinese Chemical Letters, 2025, 36(2): 110077-. doi: 10.1016/j.cclet.2024.110077
14. [14]
  Keqiang Shi , Xiujuan Hong , Dongyan Xu , Tao Pan , Huiwen Wang , Hongru Feng , Cheng Guo , Yuanjiang Pan . Analysis of RNA modifications in peripheral white blood cells from breast cancer patients by mass spectrometry. Chinese Chemical Letters, 2025, 36(3): 110079-. doi: 10.1016/j.cclet.2024.110079
15. [15]
  Wen Su , Siying Liu , Qingfu Zhang , Zhongyan Zhou , Na Wang , Lei Yue . Temperature-controlled electrospray ionization tandem mass spectrometry study on protein/small molecule interaction. Chinese Chemical Letters, 2025, 36(5): 110237-. doi: 10.1016/j.cclet.2024.110237
16. [16]
  Yongyi Li , Jin Han , Xiangyu Wang , Zhenwei Wei . In-situ reaction monitoring and kinetics study of photochemical reactions by optical focusing inductive electrospray mass spectrometry. Chinese Chemical Letters, 2025, 36(9): 110708-. doi: 10.1016/j.cclet.2024.110708
17. [17]
  Rui Su , Xiaowei Fang , Peng Zeng , Yong Qian , Xuanzhu Li , Huiyu Xing , Jiamei Lin , Jiaquan Xu . Mass spectrometry for non-destructive detection of the average diameter of micro copper wires. Chinese Chemical Letters, 2025, 36(10): 110748-. doi: 10.1016/j.cclet.2024.110748
18. [18]
  Jing-Jing Zhang , Lujun Lou , Rui Lv , Jiahui Chen , Yinlong Li , Guangwei Wu , Lingchao Cai , Steven H. Liang , Zhen Chen . Recent advances in photochemistry for positron emission tomography imaging. Chinese Chemical Letters, 2024, 35(8): 109342-. doi: 10.1016/j.cclet.2023.109342
19. [19]
  Shihong Wu , Ronghui Zhou , Hang Zhao , Peng Wu . Sonoafterglow luminescence for in vivo deep-tissue imaging. Chinese Chemical Letters, 2024, 35(10): 110026-. doi: 10.1016/j.cclet.2024.110026
20. [20]
  Feng-Qing Huang , Yu Wang , Ji-Wen Wang , Dai Yang , Shi-Lei Wang , Yuan-Ming Fan , Raphael N. Alolga , Lian-Wen Qi . Chemical isotope labeling-assisted liquid chromatography-mass spectrometry enables sensitive and accurate determination of dipeptides and tripeptides in complex biological samples. Chinese Chemical Letters, 2024, 35(11): 109670-. doi: 10.1016/j.cclet.2024.109670

Get Citation

PDF

XML

Metrics

PDF Downloads(0)
Abstract views(83)
HTML views(0)

通讯作者: 陈斌, bchen63@163.com

1.
沈阳化工大学材料科学与工程学院沈阳 110142