Lipidomic profiling of tryptophan hydroxylase 2 knockout mice reveals novel lipid biomarkers associated with serotonin deficiency

详细信息    查看全文

• 作者：Rui Weng ; Sensen Shen ; Casey Burton ; Li Yang…
• 关键词：Serotonin deficiency ; Tryptophan hydroxylase 2 knockout (Tph2−/−) mice ; Lipidomics ; Lipid biomarkers ; Two ; dimensional liquid chromatography–quadrupole time ; of ; flight mass spectrometry (2D LC–QToF ; MS)
• 刊名：Analytical and Bioanalytical Chemistry
• 出版年：2016
• 出版时间：April 2016
• 年：2016
• 卷：408
• 期：11
• 页码：2963-2973
• 全文大小：770 KB
• 参考文献：1.Berger M, Gray JA, Roth BL. The expanded biology of serotonin. Annu Rev Med. 2009;60:355–66.CrossRef
  2.Kiser D, SteemerS B, Branchi I, Homberg JR. The reciprocal interaction between serotonin and social behaviour. Neurosci Biobehav Rev. 2012;36(2):786–98.CrossRef
  3.Higley JD, Linnoila M. Low central nervous system serotonergic activity is traitlike and correlates with impulsive behavior—a nonhuman primate model investigating genetic and environmental influences on neurotransmission. Ann NY Acad Sci. 1997;836:39–56.CrossRef
  4.Rodriguez JJ, Noristani HN, Verkhratsky A. The serotonergic system in ageing and Alzheimer’s disease. Prog Neurobiol. 2012;99(1):15–41.CrossRef
  5.Igarashi M, Ma K, Gao F, Kim H-W, Rapoport SI, Rao JS. Disturbed choline plasmalogen and phospholipid fatty acid concentrations in Alzheimer’s disease prefrontal cortex. J Alzheimers Dis. 2011;24(3):507–17.
  6.Yao JK, Dougherty GG, Reddy RD, Keshavan MS, Montrose DM, Matson WR, et al. Altered interactions of tryptophan metabolites in first-episode neuroleptic-naive patients with schizophrenia. Mol Psychiatry. 2010;15(9):938–53.CrossRef
  7.Jacobsen JPR, Medvedev IO, Caron MG. The 5-HT deficiency theory of depression: perspectives from a naturalistic 5-HT deficiency model, the tryptophan hydroxylase 2(Arg)439(His) knockin mouse. Philos Trans R Soc B-Biol Sci. 2012;367(1601):2444–59.CrossRef
  8.Nichols DE, Nichols CD. Serotonin receptors. Chem Rev. 2008;108(5):1614–41.CrossRef
  9.Watkins PA, Hamilton JA, Leaf A, Spector AA, Moore SA, Anderson RE, et al. Brain uptake and utilization of fatty acids—applications to peroxisomal biogenesis diseases. J Mol Neurosci. 2001;16(2–3):87–92.CrossRef
  10.Weng R, Shen SS, Tian YL, Burton C, Xu XY, Liu Y, et al. Metabolomics approach reveals integrated metabolic network associated with serotonin deficiency. Sci Rep. 2015;5:11864.CrossRef
  11.Weng R, Shen SS, Yang L, Li M, Tian YL, Bai Y, et al. Lipidomic analysis of p-chlorophenylalanine-treated mice using continuous-flow two-dimensional liquid chromatography/quadrupole time-of-flight mass spectrometry. Rapid Commun Mass Spectrom. 2015;29(16):1491–500.CrossRef
  12.Liu Y, Jiang YA, Si YX, Kim JY, Chen ZF, Rao Y. Molecular regulation of sexual preference revealed by genetic studies of 5-HT in the brains of male mice. Nature. 2011;472(7341):95–9.CrossRef
  13.Liu Z, Zhou J, Li Y, Hu F, Lu Y, Ma M, et al. Dorsal raphe neurons signal reward through 5-HT and glutamate. Neuron. 2014;81(6):1360–74.CrossRef
  14.Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959;37(8):911–7.CrossRef
  15.Nie H, Liu R, Yang Y, Bai Y, Guan Y, Qian D, et al. Lipid profiling of rat peritoneal surface layers by online normal- and reversed-phase 2D LC QToF-MS. J Lipid Res. 2010;51(9):2833–44.CrossRef
  16.Merrill AH, Sullards MC, Allegood JC, Kelly S, Wang E. Sphingolipidomics: high-throughput, structure-specific, and quantitative analysis of sphingolipids by liquid chromatography tandem mass spectrometry. Methods. 2005;36(2):207–24.CrossRef
  17.Moore JD, Caufield WV, Shaw WA (2007) Quantitation and standardization of lipid internal standards for mass spectroscopy. In: Brown HA (ed) Lipidomics and bioactive lipids: mass-spectrometry-based lipid analysis, vol 432. Methods in enzymology. pp 351–367.
  18.Gika HG, Theodoridis GA, Wingate JE, Wilson ID. Within-day reproducibility of an HPLC-MS-Based method for metabonomic analysis: application to human urine. J Proteome Res. 2007;6(8):3291–303.CrossRef
  19.Li M, Feng BS, Liang Y, Zhang W, Bai Y, Tang W, et al. Lipid profiling of human plasma from peritoneal dialysis patients using an improved 2D (NP/RP) LC-QToF MS method. Anal Bioanal Chem. 2013;405(21):6629–38.CrossRef
  20.Want EJ, Wilson ID, Gika H, Theodoridis G, Plumb RS, Shockcor J, et al. Global metabolic profiling procedures for urine using UPLC-MS. Nat Protoc. 2010;5(6):1005–18.CrossRef
  21.Bijlsma S, Bobeldijk L, Verheij ER, Ramaker R, Kochhar S, Macdonald IA, et al. Large-scale human metabolomics studies: a strategy for data (pre-) processing and validation. Anal Chem. 2006;78(2):567–74.CrossRef
  22.Li M, Tong X, Lv P, Feng B, Yang L, Wu Z, et al. A not-stop-flow online normal-/reversed-phase two-dimensional liquid chromatography-quadrupole time-of-flight mass spectrometry method for comprehensive lipid profiling of human plasma from atherosclerosis patients. J Chromatogr A. 2014;1372:110–9.CrossRef
  23.Bradford MM. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal Biochem. 1976;72(1–2):248–54.CrossRef
  24.Lim YA, Rhein V, Baysang G, Meier F, Poljak A, Raftery MJ, et al. A beta and human amylin share a common toxicity pathway via mitochondrial dysfunction. Proteomics. 2010;10(8):1621–33.CrossRef
  25.Balboa MA, Balsinde J. Oxidative stress and arachidonic acid mobilization. Biochim Biophys Acta Mol Cell Biol Lipids. 2006;1761(4):385–91.CrossRef
  26.Yao JK, Dougherty GG, Reddy RD, Matson WR, Kaddurah-Daouk R, Keshavan MS. Associations between purine metabolites and monoamine neurotransmitters in first-episode psychosis. Front Cell Neurosci. 2013;7:90.
  27.Andrieu-Abadie N, Gouaze V, Salvayre R, Levade T. Ceramide in apoptosis signaling: relationship with oxidative stress. Free Radical Biol Med. 2001;31(6):717–28.CrossRef
  28.Goldkorn T, Ravid T, Khan EM. Life and death decisions: ceramide generation and EGF receptor trafficking are modulated by oxidative stress. Antioxid Redox Signal. 2005;7(1–2):119–28.CrossRef
  29.Latorre E, Collado MP, Fernandez I, Aragones MD, Catalan RE. Signaling events mediating activation of brain ethanolamine plasmalogen hydrolysis by ceramide. Eur J Biochem. 2003;270(1):36–46.CrossRef
  30.Lessig J, Fuchs B. Plasmalogens in biological systems: their role in oxidative processes in biological membranes, their contribution to pathological processes and aging and plasmalogen analysis. Curr Med Chem. 2009;16(16):2021–41.CrossRef
  31.Dragonas C, Bertsch T, Sieber CC, Brosche T. Plasmalogens as a marker of elevated systemic oxidative stress in Parkinson’s disease. Clin Chem Lab Med. 2009;47(7):894–7.CrossRef
  32.Kaddurah-Daouk R, McEvoy J, Baillie R, Zhu HJ, Yao JK, Nimgaonkar VL, et al. Impaired plasmalogens in patients with schizophrenia. Psychiatry Res. 2012;198(3):347–52.CrossRef
  33.Demirkan A, Isaacs A, Ugocsai P, Liebisch G, Struchalin M, Rudan I, et al. Plasma phosphatidylcholine and sphingomyelin concentrations are associated with depression and anxiety symptoms in a Dutch family-based lipidomics study. J Psychiatr Res. 2013;47(3):357–62.CrossRef
  34.Farooqui AA, Horrocks LA, Farooqui T. Glycerophospholipids in brain: their metabolism, incorporation into membranes, functions, and involvement in neurological disorders. Chem Phys Lipids. 2000;106(1):1–29.CrossRef
  35.Corda D, Iurisci C, Berrie CP. Biological activities and metabolism of the lysophosphoinositides and glycerophosphoinositols. Biochim Biophys Acta Mol Cell Biol Lipids. 2002;1582(1–3):52–69.CrossRef
  36.Corda D, Zizza P, Varone A, Filippi BM, Mariggio S. The glycerophosphoinositols: cellular metabolism and biological functions. Cell Mol Life Sci. 2009;66(21):3449–67.CrossRef
  37.Patrussi L, Mariggio S, Corde D, Baldari CT. The glycerophosphoinositols: from lipid metabolites to modulators of T-cell signaling. Front Immunol. 2013;4:213.CrossRef
  38.Luisa Doria M, Cotrim Z, Macedo B, Simoes C, Domingues P, Helguero L, et al. Lipidomic approach to identify patterns in phospholipid profiles and define class differences in mammary epithelial and breast cancer cells. Breast Cancer Res Treat. 2012;133(2):635–48.CrossRef
  39.Cui W, Cai Y, Zhou X. Advances in subunits of PI3K class I in cancer. Pathology. 2014;46(3):169–76.CrossRef
  40.Brown DA, London E. Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol. 1998;14:111–36.CrossRef
  41.Lam SM, Wang Y, Duan X, Wenk MR, Kalaria RN, Chen CP, et al. The brain lipidomes of subcortical ischemic vascular dementia and mixed dementia. Neurobiol Aging. 2014;35(10):2369–81.CrossRef
  42.Horrocks LA, Farooqui AA. Docosahexaenoic acid in the diet: its importance in maintenance and restoration of neural membrane function. Prostaglandins Leukot Essent Fatty Acids. 2004;70(4):361–72.CrossRef
  43.Cutler RG, Kelly J, Storie K, Pedersen WA, Tammara A, Hatanpaa K, et al. Involvement of oxidative stress-induced abnormalities in ceramide and cholesterol metabolism in brain aging and Alzheimer’s disease. Proc Natl Acad Sci U S A. 2004;101(7):2070–5.CrossRef
  44.Frisardi V, Panza F, Seripa D, Farooqui T, Farooqui AA. Glycerophospholipids and glycerophospholipid-derived lipid mediators: a complex meshwork in Alzheimer’s disease pathology. Prog Lipid Res. 2011;50(4):313–30.CrossRef
  45.Cheng D, Jenner AM, Shui G, Cheong WF, Mitchell TW, Nealon JR, et al. Lipid pathway alterations in Parkinson’s disease primary visual cortex. Plos ONE. 2011;6(2), e17299.CrossRef
  46.Gutknecht L, Kriegebaum C, Waider J, Schmitt A, Lesch K. Spatio-temporal expression of tryptophan hydroxylase isoforms in murine and human brain: convergent data from Tph2 knockout mice. Eur Neuropsychopharm. 2009;19(4):266–82.CrossRef
  47.Su KP, Shen WW, Huang SY. Effects of polyunsaturated fatty acids on psychiatric disorders. Am J Clin Nutr. 2000;72(5):1241. 1241.
  48.Weng R, Shen SS, Yang L, Li M, Tian YL, Bai Y, et al. Lipidomic analysis of p-chlorophenylalanine-treated mice using continuous-flow two-dimensional liquid chromatography/quadrupole time-of-flight mass spectrometry. Rapid Commun Mass Spectrom. 2015;29(16):1491–500.CrossRef
  
• 作者单位：Rui Weng (1) (2)
  Sensen Shen (1)
  Casey Burton (3)
  Li Yang (1)
  Honggang Nie (4)
  Yonglu Tian (5)
  Yu Bai (1)
  Huwei Liu (1)
  
  1. Beijing National Laboratory for Molecular Sciences, the Key Laboratory of Bioorganic Chemistry and Molecular Engineering of Ministry of Education, Institute of Analytical Chemistry, College of Chemistry and Molecular Engineering, Peking University, Beijing, 100871, China
  2. Institute of Quality Standards and Testing Technology for Agro-Products, Chinese Academy of Agriculture Sciences, Beijing, 100081, China
  3. Department of Chemistry and Center for Single Cell, Single Nanoparticle, and Single Molecule Monitoring, Missouri University of Science and Technology, Rolla, MO, 65409, USA
  4. Analytical Instrumentation Center, Peking University, Beijing, 100871, China
  5. Peking-Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, 100871, China
  
• 刊物类别：Chemistry and Materials Science
• 刊物主题：Chemistry
  Analytical Chemistry
  Food Science
  Inorganic Chemistry
  Physical Chemistry
  Monitoring, Environmental Analysis and Environmental Ecotoxicology
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1618-2650

文摘

Serotonin is an important neurotransmitter that regulates a wide range of physiological, neuropsychological, and behavioral processes. Consequently, serotonin deficiency is involved in a wide variety of neurodegenerative diseases, including Alzheimer’s disease, Parkinson’s disease, schizophrenia, and depression. The pathophysiological mechanisms underlying serotonin deficiency, particularly from a lipidomics perspective, remain poorly understood. This study therefore aimed to identify novel lipid biomarkers associated with serotonin deficiency by lipidomic profiling of tryptophan hydroxylase 2 knockout (Tph2−/−) mice. Using a high-throughput normal-/reversed-phase two-dimensional liquid chromatography–quadrupole time-of-flight mass spectrometry (NP/RP 2D LC–QToF-MS) method, 59 lipid biomarkers encompassing glycerophospholipids (glycerophosphocholines, lysoglycerophosphocholines, glycerophosphoethanolamines, lysoglycerophosphoethanolamines glycerophosphoinositols, and lysoglycerophosphoinositols), sphingolipids (sphingomyelins, ceramides, galactosylceramides, glucosylceramides, and lactosylceramides) and free fatty acids were identified. Systemic oxidative stress in the Tph2−/− mice was significantly elevated, and a corresponding mechanism that relates the lipidomic findings has been proposed. In summary, this work provides preliminary findings that lipid metabolism is implicated in serotonin deficiency.