Small molecule analysis and imaging of fatty acids in the zebra finch song system using time-of-flight-secondary ion mass spectrometry

Journal of Neurochemistry

Volumn 118, Issue 4, 2011, Pages 499-511

  Amaya, Kensey R ^a   Sweedler, Jonathan V ^b   Clayton, David F ^a,c  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c U S ARMY ENGINEER RESEARCH AND DEVELOPMENT CENTER   (United States)

Author keywords

arachidonic acid; brain; docosahexaenoic acid; imaging; SIMS; songbird

Indexed keywords

11 EICOSENOIC ACID; 11,14 EICOSADIENOIC ACID; ADRENIC ACID; ARACHIDONIC ACID; CHOLESTEROL; DIHOMO GAMMA LINOLENIC ACID; DOCOSAHEXAENOIC ACID; ESSENTIAL FATTY ACID; ICOSAPENTAENOIC ACID; LINOLEIC ACID; MYRISTIC ACID; OLEIC ACID; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; PALMITIC ACID; PALMITOLEIC ACID; STEARIC ACID; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FATTY ACID ANALYSIS; FATTY ACID SYNTHESIS; FINCH; FOREBRAIN; IMMUNOHISTOCHEMISTRY; LEARNING; LIPID COMPOSITION; MALE; MASS SPECTROMETRY; MOLECULAR DYNAMICS; NEUROCHEMISTRY; NEUROIMAGING; NONHUMAN; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; SEXUAL MATURITY; SIGNAL TRANSDUCTION; TIME OF FLIGHT SECONDARY MASS SPECTROMETRY; TISSUE DISTRIBUTION; VOCALIZATION;

ANIMALS; BRAIN CHEMISTRY; FATTY ACIDS; FATTY ACIDS, ESSENTIAL; FINCHES; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; LIPID METABOLISM; MALE; NERVE NET; PRINCIPAL COMPONENT ANALYSIS; PROSENCEPHALON; SPECTROMETRY, MASS, SECONDARY ION; VOCALIZATION, ANIMAL;

PASSERI; TAENIOPYGIA GUTTATA;

EID: 79960562787     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07274.x     Document Type: Article

References (80)

1. Adret P., and, Margoliash D., (2002) Metabolic and neural activity in the song system nucleus robustus archistriatalis: effect of age and gender. J. Comp. Neurol. 454, 409-423. (Pubitemid 35416800)
2. Altelaar A. F. M., Klinkert I., Jalink K., de Lange R. P. J., Adan R. A. H., Heeren R. M. A., and, Piersma S. R., (2006) Gold-enhanced biomolecular surface imaging of cells and tissue by SIMS and MALDI mass spectrometry. Anal. Chem. 78, 734-742. (Pubitemid 43228580)
3. Amaya K. R., Monroe E. B., Sweedler J. V., and, Clayton D. F., (2007) Lipid imaging in the zebra finch brain with secondary ion mass spectrometry. Int. J. Mass Spectrom. 260, 121-127.
4. Bazan N.G., (2005) Lipid signaling in neural plasticity, brain repair, and neuroprotection. Mol. Neurobiol. 32, 89-103. (Pubitemid 41113211)
5. Bottjer S. W., and, Altenau B., (2010) Parallel pathways for vocal learning in basal ganglia of songbirds. Nat. Neurosci. 13, 153-155.
6. Bourre J. M., Dumont O. S., Piciotti M. J., Pascal G. A., and, Durand G. A., (1992) Dietary alpha-linolenic acid deficiency in adult rats for 7 months does not alter brain docosahexaenoic acid content, in contrast to liver, heart and testes. Biochim. Biophys. Acta 1124, 119-122.
7. Brenowitz E. A., Margoliash D., and, Nordeen K. W., (1997) An introduction to birdsong and the avian song system. J. Neurobiol. 33, 495-500. (Pubitemid 27456448)
8. Brunelle A., Touboul D., and, Laprevote O., (2005) Biological tissue imaging with time-of-flight secondary ion mass spectrometry and cluster ion sources. J. Mass Spectrom. 40, 985-999. (Pubitemid 41284732)
9. Calderon F., and, Kim H. Y., (2004) Docosahexaenoic acid promotes neurite growth in hippocampal neurons. J. Neurochem. 90, 979-988. (Pubitemid 39099980)
10. Carrillo G. D., and, Doupe A. J., (2004) Is the songbird Area X striatal, pallidal, or both? An anatomical study. J. Comp. Neurol. 473, 415-437. (Pubitemid 38580458)
11. Clayton D. F., (1997) Role of gene regulation in song circuit development and song learning. J. Neurobiol. 33, 549-571. (Pubitemid 27456452)
12. Clayton D. F., and, George J. M., (1999) Synucleins in synaptic plasticity and neurodegenerative disorders. J. Neurosci. Res. 58, 120-129. (Pubitemid 29463698)
13. Clayton D. F., Balakrishnan C. N., and, London S. E., (2009) Integrating genomes, brain and behavior in the study of songbirds. Curr. Biol. 19, 865-873.
14. Cocco S., Diaz G., Stancampiano R., Diana A., Carta M., Curreli R., Sarais L., and, Fadda F., (2002) Vitamin A deficiency produces spatial learning and memory impairment in rats. Neuroscience 115, 475-482. (Pubitemid 35284765)
15. Cole-Edwards K. K., and, Bazan N. G., (2005) Lipid signaling in experimental epilepsy. Neurochem. Res. 30, 847-853. (Pubitemid 41413941)
16. Darios F., Ruipérez V., Lõpez I., Villanueva J., Gutierrez L. M., and, Davletov B., (2010) Alpha-Synuclein sequesters arachidonic acid to modulate SNARE-mediated exocytosis. EMBO Reports 11, 528-533.
17. Davletov B., and, Montecucco C., (2010) Lipid function at synapses. Curr. Opin. Neurobiol. 20, 543-549.
18. Denisenko-Nehrbass N. I., Jarvis E., Scharff C., Nottebohm F., and, Mello C. V., (2000) Site-specific retinoic acid production in the brain of adult songbirds. Neuron 27, 359-370.
19. Diau G. Y., Hsieh A. T., Sarkadi-Nagy E. A., Wijendran V., Nathanielsz P. W., and, Brenna J. T., (2005) The influence of long chain polyunsaturate supplementation on docosahexaenoic acid and arachidonic acid in baboon neonate central nervous system. BMC Med. 3, 11.
20. Ewing A. G., (2006) Molecule specific imaging in biology: what are the challenges and the important applications? Appl. Surf. Sci. 252, 6821-6826. (Pubitemid 44233805)
21. Farries M. A., and, Perkel D. J., (2002) A telencephalic nucleus essential for song learning contains neurons with physiological characteristics of both striatum and globus pallidus. J. Neurosci. 22, 3776-3787. (Pubitemid 37465782)
22. Fenton W. S., Hibbeln J., and, Knable M., (2000) Essential fatty acids, lipid membrane abnormalities, and the diagnosis and treatment of schizophrenia. Biol. Psychiatry 47, 8-21. (Pubitemid 30016075)
23. Fletcher J. S., Conlan X. A., Jones E. A., Biddulph G., Lockyer N. P., and, Vickerman J. C., (2006) TOF-SIMS analysis using C-60- effect of impact energy on yield and damage. Anal. Chem. 78, 1827-1831.
24. Forstmeier W., Segelbacher G., Mueller J. C., and, Kempenaers B., (2007) Genetic variation and differentiation in captive and wild zebra finches (Taeniopygia guttata). Mol. Ecol. 16, 4039-4050. (Pubitemid 47481041)
25. George J. M., Jin H., Woods W. S., and, Clayton D. F., (1995) Characterization of a novel protein regulated during the critical period for song learning in the zebra finch. Neuron 15, 361-372.
26. Golovko M. Y., Rosenberger T. A., Feddersen S., Faergeman N. J., and, Murphy E. J., (2007) Alpha-Synuclein gene ablation increases docosahexaenoic acid incorporation and turnover in brain phospholipids. J. Neurochem. 101, 201-211. (Pubitemid 46426477)
27. Golovko M. Y., Barcelõ-Coblijn G., Castagnet P. I., Austin S., Combs C. K., and, Murphy E. J., (2009) The role of alpha-synuclein in brain lipid metabolism: a downstream impact on brain inflammatory response. Mol. Cell. Biochem. 326, 55-66.
28. Grisham W., and, Arnold A. P., (1994) Distribution of Gaba-like immunoreactivity in the song system of the zebra finch. Brain Res. 651, 115-122. (Pubitemid 24222856)
29. Hartmann T., Kuchenbecker J., and, Grimm M. O., (2007) Alzheimer's disease: the lipid connection. J. Neurochem. 103 (Suppl. 1), 159-170.
30. Holloway C. C., and, Clayton D. F., (2001) Estrogen synthesis in the male brain triggers development of the avian song control pathway in vitro. Nat. Neurosci. 4, 170-175. (Pubitemid 32125262)
31. Innis S. M., (2008) Dietary omega 3 fatty acids and the developing brain. Brain Res. 1237, 35-43.
32. Isaac G., Pernber Z., Gieselmann V., Hansson E., Bergquist J., and, Mansson J. E., (2006) Sulfatide with short fatty acid dominates in astrocytes and neurons. FEBS J. 273, 1782-1790. (Pubitemid 43779830)
33. Israeli E., and, Sharon R., (2009) Beta-synuclein occurs in vivo in lipid-associated oligomers and forms hetero-oligomers with alpha-synuclein. J. Neurochem. 108, 465-474.
34. Jeong J. K., Velho T. A. F., and, Mello C. V., (2005) Cloning and expression analysis of retinoic acid receptors in the zebra finch brain. J. Comp. Neurol. 489, 23-41. (Pubitemid 40934671)
35. Jin H., and, Clayton D. F., (1997) Synelfin regulation during the critical period for song learning in normal and isolated juvenile zebra finches. Neurobiol. Learn. Mem. 68, 271-284. (Pubitemid 27506323)
36. Johansson B., (2006) ToF-SIMS imaging of lipids in cell membranes. Surf. Interface Anal. 38, 1401-1412. (Pubitemid 44729087)
37. Johnson F., Sablan M. M., and, Bottjer S. W., (1995) Topographic organization of a forebrain pathway involved with vocal learning in zebra finches. J. Comp. Neurol. 358, 260-278.
38. Kim K., Yang J., and, Kim E., (2010) Diacylglycerol kinases in the regulation of dendritic spines. J. Neurochem. 112, 577-587.
39. Konishi M., and, Akutagawa E., (1985) Neuronal growth, atrophy and death in a sexually dimorphic song nucleus in the zebra finch brain. Nature 315, 145-147. (Pubitemid 15064533)
40. Krezel W., Ghyselinck N., Abdel T., Dupe V., Kastner P., Borelli E., and, Chambon P., (1998) Impaired locomotion and dopamine signaling in retinoid receptor mutant mice. Science 279, 863-867. (Pubitemid 28106280)
41. Kulp K. S., Berman E. S., Knize M. G., Shattuck D. L., Nelson E. J., Wu L., Montgomery J. L., Felton J. S., and, Wu K. J., (2006) Chemical and biological differentiation of three human breast cancer cell types using time-of-flight secondary ion mass spectrometry. Anal. Chem. 78, 3651-3658. (Pubitemid 43848958)
42. Lindon J. C., Nicholson J. K., and, Holmes E., (2007) The Handbook of Metabonomics and Metabolomics. Elsevier, Amsterdam, Oxford.
43. London S. E., Monks D. A., Wade J., and, Schlinger B. A., (2006) Widespread capacity for steroid synthesis in the avian brain and song system. Endocrinology 147, 5975-5987. (Pubitemid 44833516)
44. Lovell P. V., Clayton D. F., Replogle K. L., and, Mello C. V., (2008) Birdsong "transcriptomics": neurochemical specializations of the oscine song system. PLoS ONE 3, e3440.
45. Maier O., Oberle V., and, Hoekstra D., (2002) Fluorescent lipid probes: some properties and applications (a review). Chem. Phys. Lipids 116, 3-18. (Pubitemid 34686984)
46. Maldjian A., Cristofori C., Noble R., and, Speake B. K., (1996) The fatty acid composition of brain phospholipids from chicken and duck embryos. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 115, 153-158. (Pubitemid 26364288)
47. Martin R. E., and, Bazan N. G., (1992) Changing fatty acid content of growth cone lipids prior to synaptogenesis. J. Neurochem. 59, 318-325.
48. Mas S., Perez R., Martinez-Pinna R., Egido J., and, Vivanco F., (2008) Cluster TOF-SIMS imaging: a new light for in situ metabolomics? Proteomics 8, 3735-3745.
49. McDonnell L. A., Piersma S. R., Altelaar A. F. M., Mize T. H., Luxembourg S. L., Verhaert P. D. E. M., van Minnen J., and, Heeren R. M. A., (2005) Subcellular imaging mass spectrometry of brain tissue. J. Mass Spectrom. 40, 160-168. (Pubitemid 40330922)
50. McGee C. D., Greenwood C. E., and, Cinader B., (1994) Dietary fat composition and age affect synaptosomal and retinal phospholipid fatty acid composition in C57BL/6 mice. Lipids 29, 605-610. (Pubitemid 24282368)
51. Mello C. V., (2002) Mapping vocal communication pathways in birds with inducible gene expression. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 188, 943-959. (Pubitemid 36251489)
52. Monroe E. B., Jurchen J. C., Lee J., Rubakhin S. S., and, Sweedler J. V., (2005) Vitamin E imaging and localization in the neuronal membrane. J. Am. Chem. Soc. 127, 12152-12153. (Pubitemid 41279202)
53. Monroe E.B., Annangudi S.P., Hatcher N.G., Gutstein H.B., Rubakhin S.S., and, Sweedler J.V., (2008) SIMS and MALDI MS imaging of the spinal cord. Proteomics 8, 3746-3754.
54. Moriguchi T., Greiner R. S., and, Salem N., Jr, (2000) Behavioral deficits associated with dietary induction of decreased brain docosahexaenoic acid concentration. J. Neurochem. 75, 2563-2573.
55. Nygren H., Malmberg P., Kriegeskotte C., and, Arlinghaus H. F., (2004) Bioimaging TOF-SIMS: localization of cholesterol in rat kidney sections. FEBS Lett. 566, 291-293. (Pubitemid 38625974)
56. Oster T., and, Pillot T., (2010) Docosahexaenoic acid and synaptic protection in Alzheimer's disease mice. BBA-Mol. Cell Bio. L. 1801, 791-798.
57. Ostrowski S. G., Szakal C., Kozole J., Roddy T. P., Xu J. Y., Ewing A. G., and, Winograd N., (2005) Secondary ion MS imaging of lipids in picoliter vials with a buckminsterfullerene ion source. Anal. Chem. 77, 6190-6196. (Pubitemid 41436952)
58. Pernber Z., Richter K., Mansson J. E., and, Nygren H., (2007) Sulfatide with different fatty acids has unique distributions in cerebellum as imaged by time-of-flight secondary ion mass spectrometry (TOF-SIMS). Biochim. Biophys. Acta 1771, 202-209. (Pubitemid 46210191)
59. Pinaud R., and, Mello C. V., (2007) GABA immunoreactivity in auditory and song control brain areas of zebra finches. J. Chem. Neuroanat. 34, 1-21. (Pubitemid 47002218)
60. Piomelli D., (2003) The molecular logic of endocannabinoid signalling. Nat. Rev. Neurosci. 4, 873-884. (Pubitemid 37351427)
61. Reiner A., Laverghetta A. V., Meade C. A., Cuthbertson S. L., and, Bottjer S. W., (2004) An immunohistochemical and pathway tracing study of the striatopallidal organization of area X in the male zebra finch. J. Comp. Neurol. 469, 239-261. (Pubitemid 38083873)
62. Replogle K., Arnold A. P., Ball G. F., et al. (2008) The Songbird Neurogenomics (SoNG) Initiative: community-based tools and strategies for study of brain gene function and evolution. BMC Genomics 9, 131.
63. Sanchez-Mejia R. O., and, Mucke L., (2010) Phospholipase A2 and arachidonic acid in Alzheimer's disease. BBA-Mol. Cell Bio. L. 1801, 784-790.
64. Sastry P. S., (1985) Lipids of nervous tissue: composition and metabolism. Prog. Lipid Res. 24, 69-176.
65. Simopoulos A. P., (2002) Omega-3 fatty acids in inflammation and autoimmune diseases. J. Am. Coll. Nutr. 21, 495-505. (Pubitemid 36026261)
66. Sjovall P., Lausmaa J., and, Johansson B., (2004) Mass spectrometric imaging of lipids in brain tissue. Anal. Chem. 76, 4271-4278. (Pubitemid 39013993)
67. Soderstrom K., Tian Q., Valenti M., and, Di Marzo V., (2004) Endocannabinoids link feeding state and auditory perception-related gene expression. J. Neurosci. 24, 10013-10021. (Pubitemid 39463583)
68. Sodhi R. N. S., (2004) Time-of-flight secondary ion mass spectrometry (TOF-SIMS): versatility in chemical and imaging surface analysis. Analyst 129, 483-487. (Pubitemid 38813511)
69. Speake B. K., and, Wood N. A. R., (2005) Timing of incorporation of docosahexaenoic acid into brain and muscle phospholipids during precocial and altricial modes of avian development. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 141, 147-158. (Pubitemid 40797939)
70. Suzuki T., (2002) Lipid rafts at postsynaptic sites: distribution, function and linkage to postsynaptic density. Neurosci. Res. 44, 1-9. (Pubitemid 36158698)
71. Tahallah N., Brunelle A., De La Porte S., and, Laprevote O., (2008) Lipid mapping in human dystrophic muscle by cluster-time-of-flight secondary ion mass spectrometry imaging. J. Lipid Res. 49, 438-454. (Pubitemid 351213629)
72. Tchernichovski O., Mitra P. P., Lints T., and, Nottebohm F., (2001) Dynamics of the vocal imitation process: how a zebra finch learns its song. Science 291, 2564-2569. (Pubitemid 32249674)
73. Touboul D., Brunelle A., Halgand F., De La Porte S., and, Laprevote O., (2005) Lipid imaging by gold cluster time-of-flight secondary ion mass spectrometry: application to Duchenne muscular dystrophy. J. Lipid Res. 46, 1388-1395. (Pubitemid 43109802)
74. Turner N., (2005) An allometric comparison of microsomal membrane lipid composition and sodium pump molecular activity in the brain of mammals and birds. J. Exp. Biol. 208, 371-381. (Pubitemid 40307239)
75. Wagner M. S., Graham D. J., Ratner B. D., and, Castner D. G., (2004) Maximizing information obtained from secondary ion mass spectra of organic thin films using multivariate analysis. Surf. Sci. 570, 78-97.
76. Warren W. C., Clayton D. F., Ellegren H., et al. (2010) The genome of a songbird. Nature 464, 757-762.
77. Williams J. H., Errington M. L., Lynch M. A., and, Bliss T. V., (1989) Arachidonic acid induces a long-term activity-dependent enhancement of synaptic transmission in the hippocampus. Nature 341, 739-742. (Pubitemid 19260887)
78. Wu L., Lu X., Kulp K. S., Knize M. G., Berman E. S. F., Nelson E. J., Felton J. S., and, Wu K. J. J., (2007) Imaging and differentiation of mouse embryo tissues by ToF-SIMS. Int. J. Mass Spectrom., 260, 137.
79. Zeigler H. P., and, Marler P., (2004) Behavioral Neurobiology Of Bird Song (Annals of the New York Academy of Sciences Vol. 1016). New York Academy of Sciences, New York.
80. Zhang Y., Appelkvist E. L., Kristensson K., and, Dallner G., (1996) The lipid compositions of different regions of rat brain during development and aging. Neurobiol. Aging 17, 869-875. (Pubitemid 27022740)