Metabolomic screening of regional brain alterations in the APP/PS1 transgenic model of Alzheimer's disease by direct infusion mass spectrometry

Journal of Pharmaceutical and Biomedical Analysis

Volumn 102, Issue , 2015, Pages 425-435

  González Domínguez, Raúl ^a   García Barrera, Tamara ^a   Vitorica, Javier ^b,c,d   Gómez Ariza, José Luis ^a  

^a UNIVERSITY OF HUELVA   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

^c CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^d Instituto de Biomedicina de Sevilla   (Spain)

Author keywords

Alzheimer's disease; APP PS1 mice; Brain regions; Direct infusion mass spectrometry; Metabolomics

Indexed keywords

AMINO ACID; AMYLOID PRECURSOR PROTEIN; ETHANOLAMINE; FATTY ACID; INOSITOL; LIPID; NUCLEOTIDE; PHOSPHOLIPID; PRESENILIN 1; PURINE; PYRIMIDINE; SERINE; STEROL; AMYLOID BETA-PROTEIN PRECURSOR; PRESENILIN 1, MOUSE; PRESENILIN-1;

ALZHEIMER DISEASE; AMINO ACID METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN METABOLISM; BRAIN TISSUE; CEREBELLUM; COGNITIVE DEFECT; CONTROLLED STUDY; DIRECT INFUSION MASS SPECTROMETRY; ENERGY CONSERVATION; FEMALE; HIGH THROUGHPUT SCREENING; HIPPOCAMPUS; HOMEOSTASIS; MALE; MASS SPECTROMETRY; METABOLITE; METABOLOMICS; MOUSE; NEUROPATHOLOGY; NEUROTRANSMISSION; NONHUMAN; NUCLEOTIDE METABOLISM; OLFACTORY BULB; OXIDATIVE STRESS; PATHOGENESIS; TRANSGENIC ORGANISM; WILD TYPE; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; GENETICS; METABOLISM; METHODS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; FEMALE; MALE; MASS SPECTROMETRY; METABOLOMICS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PRESENILIN-1;

EID: 84911163843     PISSN: 07317085     EISSN: 1873264X     Source Type: Journal    
DOI: 10.1016/j.jpba.2014.10.009     Document Type: Article

References (68)

1. Hall A.M., Roberson E.D. Mouse models of Alzheimer's disease. Brain Res. Bull. 2012, 88:3-12.
2. Malm T., Koistinaho J., Kanninen K. Utilization of APPswe/PS1dE9 transgenic mice in research of Alzheimer's disease: focus on gene therapy and cell-based therapy applications. Int. J. Alzheimers Dis. 2011, 2011:517160.
3. Filalia M., Lalonde R. Age-related cognitive decline and nesting behavior in an APPswe/PS1 bigenic model of Alzheimer's disease. Brain Res. 2009, 1292:93-99.
4. Lindon J.C., Holmes E., Nicholson J.K. Metabonomics and its role in drug development and disease diagnosis. Expert Rev. Mol. Diagn. 2004, 4:189-199.
5. 1H MRS in APP/PS1 mice. Neurobiol. Aging 2008, 29:1423-1433.
6. Xu W., Zhan Y., Huang W., Wang X., Zhang S., Lei H. Reduction of hippocampal N-acetyl aspartate level in aged APPSwe/PS1dE9 transgenic mice is associated with degeneration of CA3 pyramidal neurons. J. Neurosci. Res. 2010, 88:3155-3160.
7. Chen S.Q., Cai Q., Shen Y.Y., Wang P.J., Teng G.J., Zhang W., Zang F.C. Age-related changes in brain metabolites and cognitive function in APP/PS1 transgenic mice. Behav. Brain Res. 2012, 235:1-6.
8. Dedeoglu A., Choi J.K., Cormier K., Kowall N.W., Jenkins B.G. Magnetic resonance spectroscopic analysis of Alzheimer's disease mouse brain that express mutant human APP shows altered neurochemical profile. Brain Res. 2004, 1012:60-65.
9. 1H MRS in vitro. NMR Biomed. 2012, 25:52-58.
10. 1H NMR metabolomics investigation of an Alzheimer's disease (AD) mouse model pinpoints important biochemical disturbances in brain and plasma. Metabolomics 2013, 9:974-983.
11. Salek R.M., Xia J., Innes A., Sweatman B.C., Adalbert R., Randle S., McGowan E., Emson P.C., Griffin J.L. A metabolomic study of the CRND8 transgenic mouse model of Alzheimer's disease. Neurochem. Int. 2010, 56:937-943.
12. 1H HR-MAS. Behav. Brain Res. 2010, 211:125-131.
13. 1H NMR metabolomic signatures in five brain regions of the AβPPswe Tg2576 mouse model of Alzheimer's disease at four ages. J. Alzheimers Dis. 2014, 39:121-143.
14. Dettmer K., Aronov P.A., Hammock B.D. Mass spectrometry-based metabolomics. Mass Spectrom. Rev. 2007, 26:51-78.
15. Piro J.R., Benjamin D.I., Duerr J.M., Pi Y.Q., Gonzales C., Wood K.M., Schwartz J.W., Nomura D.K., Samad T.A. A dysregulated endocannabinoid-eicosanoid network supports pathogenesis in a mouse model of Alzheimer's disease. Cell Rep. 2012, 1:617-623.
16. Hu Z.P., Browne E.R., Liu T., Angel T.E., Ho P.C., Chan E.C.Y. Metabonomic profiling of TASTPM transgenic alzheimer's disease mouse model. J. Proteome Res. 2012, 11:5903-5913.
17. Trushina E., Nemutlu E., Zhang S., Christensen T., Camp J., Mesa J., Siddiqui A., Tamura Y., Sesaki H., Wengenack T.M., Dzeja P.P., Poduslo J.F. Defects in mitochondrial dynamics and metabolomic signatures of evolving energetic stress in mouse models of familial Alzheimer's disease. PLoS ONE 2012, 7:e32737.
18. Wang H., Lian K., Han B., Wang Y., Kuo S.H., Geng Y., Qiang J., Sun M., Wang M. Age-related alterations in the metabolic profile in the hippocampus of the senescence-accelerated mouse prone 8: a spontaneous Alzheimer's disease mouse model. J. Alzheimers Dis. 2014, 39:841-848.
19. Draper J., Lloyd A.J., Goodacre R., Beckmann M. Flow infusion electrospray ionisation mass spectrometry for high throughput, non-targeted metabolite fingerprinting: a review. Metabolomics 2013, 9:S4-S29.
20. Lin S., Liu H., Kanawati B., Liu L., Dong J., Li M., Huang J., Schmitt-Kopplin P., Cai Z. Hippocampal metabolomics using ultrahigh-resolution mass spectrometry reveals neuroinflammation from Alzheimer's disease in CRND8 mice. Anal. Bioanal. Chem. 2013, 405:5105-5117.
21. Lin S., Kanawati B., Liu L., Witting M., Li M., Huang J., Schmitt-Kopplin P., Cai Z. Ultra high resolution mass spectrometry-based metabolic characterization reveals cerebellum as a disturbed region in two animal models. Talanta 2014, 118:45-53.
22. Jankowsky J.L., Fadale D.J., Anderson J., Xu G.M., Gonzales V., Jenkins N.A., Copeland N.G., Lee M.K., Younkin L.H., Wagner S.L., Younkin S.G., Borchelt D.R. Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: evidence for augmentation of a 42-specific g secretase. Hum. Mol. Genet. 2004, 13:159-170.
23. Sangster T., Major H., Plumb R., Wilson A.J., Wilson I.D. A pragmatic and readily implemented quality control strategy for HPLC-MS and GC-MS-based metabonomic analysis. Analyst 2006, 131:1075-1078.
24. van den Berg R.A., Hoefsloot H.C.J., Westerhuis J.A., Smilde A.K., van der Werf M.J. Centering, scaling, and transformations: improving the biological information content of metabolomics data. BMC Genomics 2006, 7:142.
25. Pulfer M., Murphy R.C. Electrospray mass spectrometry of phospholipids. Mass Spectrom. Rev. 2003, 22:332-364.
26. Wang C., Xie S., Yang J., Yang Q., Xu G. Structural identification of human blood phospholipids using liquid chromatography/quadrupole-linear ion trap mass spectrometry. Anal. Chim. Acta 2004, 525:1-10.
27. Vernez L., Hopfgartner G., Wenk M., Krahenbuhl S. Determination of carnitine and acylcarnitines in urine by high-performance liquid chromatography-electrospray ionization ion trap tandem mass spectrometry. J. Chromatogr. A 2003, 984:203-213.
28. Xia J., Wishart D.S. MetPA: a web-based metabolomics tool for pathway analysis and visualization. Bioinformatics 2010, 26:2342-2344.
29. Lin L., Yu Q., Yan X., Hang W., Zheng J., Xing J., Huang B. Direct infusion mass spectrometry or liquid chromatography mass spectrometry for human metabonomics? A serum metabonomic study of kidney cancer. Analyst 2010, 135:2970-2978.
30. Lokhov P.G., Dashtiev M.I., Moshkovskii S.A., Archakov A.I. Metabolite profiling of blood plasma of patients with prostate cancer. Metabolomics 2010, 6:156-163.
31. Lokhov P.G., Kharybin O.N., Archakov A.I. Diagnosis of lung cancer based on direct-infusion electrospray mass spectrometry of blood plasma metabolites. Int. J. Mass Spectrom. 2012, 309:200-205.
32. Gonzalez-Dominguez R., Garcia-Barrera T., Gomez-Ariza J.L. Metabolomic approach to Alzheimer's disease diagnosis based on mass spectrometry. Chem. Papers 2012, 66:829-835.
33. Gonzalez-Dominguez R., Garcia-Barrera T., Gomez-Ariza J.L. Combination of metabolomic and phospholipid-profiling approaches for the study of Alzheimer's disease. J. Proteomics 2014, 104:37-47.
34. González-Domínguez R., García-Barrera T., Gómez-Ariza J.L. Metabolomic study of lipids in serum for biomarker discovery in Alzheimer's disease using direct infusion mass spectrometry. J. Pharm. Biomed. Anal. 2014, 98:321-326.
35. 2. Neurochem. Res. 2004, 29:1961-1977.
36. Walter A., Korth U., Hilgert M., Hartmann J., Weichel O., Hilgert M., Fassbender K., Schmitt A., Klein J. Glycerophosphocholine is elevated in cerebrospinal fluid of Alzheimer patients. Neurobiol. Aging 2004, 25:1299-1303.
37. Frisardi V., Panza F., Seripa D., Farooqui T., Farooqui A.A. Glycerophospholipids and glycerophospholipid-derived lipid mediators: a complex meshwork in Alzheimer's disease pathology. Prog. Lipid Res. 2011, 50:313-330.
38. Yao J.K., Wengenack T.M., Curran G.L., Poduslo J.F. Reduced membrane lipids in the cortex of Alzheimer's disease transgenic mice. Neurochem. Res. 2009, 34:102-108.
39. Han X., Holtzman D.M. McKeel Jr DW. Plasmalogen deficiency in early Alzheimer's disease subjects and in animal models: molecular characterization using electrospray ionization mass spectrometry. J. Neurochem. 2001, 77:1168-1180.
40. Chan R.B., Oliveira T.G., Cortes E.P., Honig L.S., Duff K.E., Small S.A., Wenk M.R., Shui G., Di Paolo G. Comparative lipidomic analysis of mouse and human brain with Alzheimer disease. J. Biol. Chem. 2012, 287:2678-2688.
41. Kou J., Kovacs G.G., Höftberger R., Kulik W., Brodde A., Forss-Petter S., Hönigschnabl S., Gleiss A., Brügger B., Wanders R., Just W., Budka H., Jungwirth S., Fischer P., Berger J. Peroxisomal alterations in Alzheimer's disease. Acta Neuropathol. 2011, 122:271-283.
42. Axelsen P.H., Murphy R.C. Quantitative analysis of phospholipids containing arachidonate and docosahexaenoate chains in microdissected regions of mouse brain. J. Lipid Res. 2010, 51:660-671.
43. 1H NMR analysis of the polar metabolome of post-mortem brain tissue. Metabolomics 2014, 10:744-753.
44. Makar T.K., Cooper A.J., Tofel-Grehl B., Thaler H.T., Blass J.P. Carnitine, carnitine acetyltransferase, and glutathione in Alzheimer brain. Neurochem. Res. 1995, 20:705-711.
45. Yao J., Hamilton R.T., Cadenas E., Brinton R.D. Decline in mitochondrial bioenergetics and shift to ketogenic profile in brain during reproductive senescence. Biochim. Biophys. Acta 2010, 1800:1121-1126.
46. Yang S.Y., He X.Y., Schulz H. 3-Hydroxyacyl-CoA dehydrogenase and short chain 3-hydroxyacyl-CoA dehydrogenase in human health and disease. FEBS J. 2005, 272:4874-4883.
47. Cuadrado-Tejedor M., Cabodevilla J.F., Zamarbide M., Gómez-Isla T., Franco R., Perez-Mediavilla A. Age-related mitochondrial alterations without neuronal loss in the hippocampus of a transgenic model of Alzheimer's disease. Curr. Alzheimer Res. 2013, 10:390-405.
48. Parnetti L., Gaiti A., Polidori M.C., Brunetti M., Palumbo B., Chionne F., Cadini D., Cecchetti R., Senin U. Increased cerebrospinal fluid pyruvate levels in Alzheimer's disease. Neurosci. Lett. 2005, 199:231-233.
49. Sims B., Powers R.E., Sabina R.L., Theibert A.B. Elevated adenosine monophosphate deaminase activity in Alzheimer's disease brain. Neurobiol. Aging 1998, 19:385-391.
50. Cai Z., Yan L.J., Li K., Quazi S.H., Zhao B. Roles of AMP-activated protein kinase in Alzheimer's disease. Neuromol. Med. 2012, 14:1-14.
51. Albasanz J.L., Perez S., Barrachina M., Ferrer I., Martín M. Up-regulation of adenosine receptors in the frontal cortex in Alzheimer's disease. Brain Pathol. 2008, 18:211-219.
52. Angulo E., Casadó V., Mallol J., Canela E.I., Viñals F., Ferrer I., Lluis C., Franco R. A1 adenosine receptors accumulate in neurodegenerative structures in Alzheimer's disease and mediate both amyloid precursor protein processing and tau phosphorylation and translocation. Brain Pathol. 2003, 13:440-451.
53. Czech C., Berndt P., Busch K., Schmitz O., Wiemer J., Most V., Hampel H., Kastler J., Senn H. Metabolite profiling of Alzheimer's disease cerebrospinal fluid. PLoS ONE 2012, 7:e31501.
54. Lyras L., Cairns N.J., Jenner A., Jenner P., Halliwell B. An assessment of oxidative damage to proteins, lipids, and DNA in brain from patients with Alzheimer's disease. J. Neurochem. 1997, 68:2061-2069.
55. Gabbita S.P., Lovell M.A., Markesbery W.R. Increased nuclear DNA oxidation in the brain in Alzheimer's disease. J. Neurochem. 1998, 71:2034-2040.
56. Fabelo N., Martín V., Marín R., Santpere G., Aso E., Ferrer I., Díaz M. Evidence for premature lipid raft aging in APP/PS1 double-transgenic mice, a model of familial Alzheimer disease. J. Neuropathol. Exp. Neurol. 2012, 71:868-881.
57. Strott C.A., Higashi Y. Cholesterol sulfate in human physiology: what's it all about. J. Lipid Res. 2003, 44:1268-1278.
58. Ramalho R.M., Viana R.J.S., Low W.C., Steer C.J., Rodrigues C.M.P. Bile acids and apoptosis modulation: an emerging role in experimental Alzheimer's disease. Trends Mol. Med. 2008, 14:54-62.
59. Lo A.C., Callaerts-Vegh Z., Nunes A.F., Rodrigues C.M.P., D'Hooge R. Tauroursodeoxycholic acid (TUDCA) supplementation prevents cognitive impairment and amyloid deposition in APP/PS1 mice. Neurobiol. Dis. 2013, 50:21-29.
60. Storga D., Vrecko K., Birkmayer J.G.D., Reibnegger G. Monoaminergic neurotransmitters, their precursors and metabolites in brains of Alzheimer patients. Neurosci. Lett. 1996, 203:29-32.
61. Fonteh A.N., Harrington R.J., Tsai A., Liao P., Harrington M.G. Free amino acid and dipeptide changes in the body fluids from Alzheimer's disease subjects. Amino Acids 2007, 32:213-224.
62. Samakashvili S., Ibáñez C., Simó C., Gil-Bea F.J., Winblad B., Cedazo-Mínguez A., Cifuentes A. Analysis of chiral amino acids in cerebrospinal fluid samples linked to different stages of Alzheimer disease. Electrophoresis 2011, 32:2757-2764.
63. Yatin S.M., Yatin M., Varadarajan S., Ain K.B., Butterfield D.A. Role of spermine in amyloid β-peptide-associated free radical-induced neurotoxicity. J. Neurosci. Res. 2001, 63:395-401.
64. Inoue K., Tsutsui H., Akatsu H., Hashizume Y., Matsukawa N., Yamamoto T., Toyo'oka T. Metabolic profiling of Alzheimer's disease brains. Sci. Rep. 2013, 3:2364.
65. Hansmannel F., Sillaire A., Kamboh M.I., Lendon C., Pasquier F., Hannequin D., Laumet G., Mounier A., Ayral A.M., DeKosky S.T., Hauw J.J., Berr C., Mann D., Amouyel P., Campion D., Lambert J.C. Is the urea cycle involved in Alzheimer's disease. J. Alzheimers Dis. 2010, 21:1013-1021.
66. Perry T.L., Yong V.W., Bergeron C., Hansen S., Jones K. Amino acids, glutathione, and glutathione transferase activity in the brains of patients with Alzheimer's disease. Ann. Neurol. 1987, 21:331-336.
67. Aoyama K., Nakaki T. Impaired glutathione synthesis in neurodegeneration. Int. J. Mol. Sci. 2013, 14:21021-21044.
68. Adams J.D., Klaidman L.K., Odunze I.N., Shen H.C., Miller C.A. Alzheimer's and Parkinson's disease. Brain levels of glutathione, glutathione disulfide, and vitamin E. Mol. Chem. Neuropathol. 1991, 14:213-226.